Use of soil actinomycetes for pharmaceutical, food, agricultural, and environmental purposes

Abstract

In this article, we reviewed the international scientific production of the last years on actinomycetes isolated from soil aiming to report recent advances in using these microorganisms for different applications. The most promising genera, isolation conditions and procedures, pH, temperature, and NaCl tolerance of these bacteria were reported. Based on the content analysis of the articles, most studies have focused on the isolation and taxonomic description of new species of actinomycetes. Regarding the applications, the antimicrobial potential (antibacterial and antifungal) prevailed among the articles, followed by the production of enzymes (cellulases and chitinases, etc.), agricultural uses (plant growth promotion and phytopathogen control), bioremediation (organic and inorganic contaminants), among others. Furthermore, a wide range of growth capacity was verified, including temperatures from 4 to 60 °C (optimum: 28 °C), pH from 3 to 13 (optimum: 7), and NaCl tolerance up to 32% (optimum: 0–1%), which evidence a great tolerance for actinomycetes cultivation. Streptomyces was the genus with the highest incidence among the soil actinomycetes and the most exploited for different uses. Besides, the interest in isolating actinomycetes from soils in extreme environments (Antarctica and deserts, for example) is growing to explore the adaptive capacities of new strains and the secondary metabolites produced by these microorganisms for different industrial interests, especially for pharmaceutical, food, agricultural, and environmental purposes.

Introduction

Actinomycetes are spore-forming and Gram-positive bacteria belonging to the phylum Actinobacteria, which can be found in soils, aquatic environments, air, and even in extreme environments, such as deserts, deep-sea sediments, and Antarctica (Abdelmohsen et al. 2015; Arifiyanto et al. 2020; Barka et al. 2015; Bhatti et al. 2017; Kim et al. 2020; Meliani et al. 2022; Rajivgandhi et al. 2022; Sarkar and Suthindhiran 2022; Selim et al. 2021; Su et al. 2022; Ul-Hassan and Wellington 2009). In their DNA, actinomycetes contain a high G + C ratio (guanine + cytosine) between 57 and 75% (Barka et al. 2015; Bhatti et al. 2017; Ul-Hassan and Wellington 2009). Actinomycetes have fungal characteristics, as they form hyphae and spores like fungi, but due to their prokaryote cell are classified as bacteria in the kingdom Monera (Alqahtani et al. 2022; Barka et al. 2015; Bhatti et al. 2017; Rajivgandhi et al. 2022).

Most of the actinomycetes are aerobic, chemoheterotrophic, and mesophilic (Barka et al. 2015; Bhatti et al. 2017). It is estimated that soils have 10⁴ to 10⁸ actinomycetes/g soil, mainly in alkaline soils with a high concentration of organic matter (Barka et al. 2015; Bhatti et al. 2017). In soil, actinomycetes collaborate with several processes, such as nitrogen fixation, phosphate solubilization, production of phytohormones and enzymes, organic matter decomposition, biocontrol of phytopathogens, bioremediation, among others (AbdElgawad et al. 2020; Bhatti et al. 2017; Bouizgarne 2022; Farda et al. 2022; Fu et al. 2022; Hozzein et al. 2019; Ruangwong et al. 2022). The best growing conditions for most actinomycetes are temperature between 25 and 30 °C, neutral pH (6 to 8) and low moisture content (Barka et al. 2015; Bhatti et al. 2017). However, actinomycetes can grow under unfavorable conditions (Farda et al. 2022).

These bacteria are known for producing several important secondary metabolites for medicine, food industry, and agriculture and are widely used and studied for obtaining antibiotics, antifungals, antivirals, immunosuppressants, compounds with anticancer and antioxidant activity, enzymes, bioinsecticides, biostimulants, biosurfactants, among other applications (Arifiyanto et al. 2020; Barka et al. 2015; Bhatti et al. 2017; Devi et al. 2022; Fu et al., 2022; Meliani et al. 2022; Osama et al., 2022; Rajivgandhi et al. 2022; Sarkar and Suthindhiran 2022; Selim et al. 2021; Ul-Hassan and Wellington 2009). About 23,000 secondary metabolites are produced by microorganisms, it is estimated that 45% are produced by actinomycetes (Kim et al. 2020; Olano et al. 2008). However, it is estimated that only 1% of actinomycetes species has been cultivated (Kumar et al. 2019).

To the best of our knowledge, few review articles comprehensively address the different potentials of actinomycetes. Bhatti et al. (2017) explored the role of actinomycetes in soil quality and plant health, their occurrence in marine and terrestrial environments, and their potential to produce bioproducts of environmental, agricultural and food interest. Javed et al. (2021) and Bouizgarne (2022) focused on the potential application of actinomycetes in the agricultural context. Ravi and Kannabiran (2018) reviewed the production of bioactive secondary metabolites from actinomycetes isolated from Indian Peninsula marine soils. Selim et al. (2021) addressed their work by presenting the environments in which actinomycetes are more commonly found and the secondary metabolites produced by these microorganisms. Farda et al. (2022) reviewed the diversity and biotechnological properties of actinomycetes isolated from caves.

In this context, this work aimed to synthesize the international scientific production on actinomycetes isolated from soils to present their applications for pharmaceutical, food, agriculture and environmental purposes, the promising genera for each potential use, and the growth and cultivation conditions of these microorganisms.

Overview of the soil actinomycetes

The genus Streptomyces predominated among the analyzed articles, identified in more than 100 papers. According to Farda et al. (2022), Streptomyces is the most studied genus of actinomycetes. In the sequence, appear Nocardia and Nonomuraea with 14 mentions each. The genus Amycolatopsis was explored in 9 studies, while Micromonospora and Streptosporangium in 7 articles each. In addition, 45 different genera of actinomycetes were identified, but these did not have more than 6 mentions among the analyzed studies. On the other hand, there was no taxonomic identification of actinomycetes in 41 articles.

It is estimated that Streptomyces represents about 50% of the actinomycetes population in the soil, containing more than 500 species described and isolated from different environmental compartments (Gopalakrishnan et al. 2020; Meliani et al. 2022). This genus has several applications of pharmaceutical, agricultural and environmental interest since they: a) are important producing sources of antibiotics, enzymes and other secondary metabolites; b) favor the growth of plants by facilitating the assimilation of nutrients and minerals; c) are biological controllers of pests and diseases that impact numerous agricultural crops; d) can be used in bioremediation processes (Chater 2013; Gopalakrishnan et al. 2020; Meliani et al. 2022; Sarkar and Suthindhiran 2022; Sharma et al. 2020).

The genus Nocardia is widely explored by the scientific community for obtaining bioactive compounds, secondary metabolites production and application as agents for pathogens control (Nikou et al. 2015; Sharma et al. 2016; Zhang et al. 2019). However, some species of this genus can cause disease in animals and humans (Grange et al. 2012; Ribeiro et al. 2008). Members of the Nonomuraea genus are non-acid-fast bacteria that form extensively branched substrate and aerial mycelia (Kämpfer 2015). Nonomuraea species have been isolated from soils, sediments, plants, mangroves, caves, and some species are resistant to the presence of heavy metals and are capable of producing enzymes and compounds with anticancer and antimicrobial activity (Hamedi et al. 2015a; Huang et al. 2018; Nakaew et al. 2012; Pudjirahart et al. 2011).

Regarding growth parameters, temperature, pH, and NaCl tolerance are the main parameters evaluated in studies on actinomycetes. Based on the analysis of 264 articles, it is possible to verify the growth capacity of these microorganisms in a wide range for each of these parameters. There were reports of actinomycetes capable of growing from 4 to 60 °C (Huang et al. 2017; Tang et al. 2019; Wu et al. 2016; Zhang et al. 2019). However, the optimum growth temperature verified for actinomycetes was 28 °C. Furthermore, some actinomycetes are able to grow in culture media with pH values of 3 and 13 (Penkhrue et al. 2018; Song et al. 2019). However, the pH range most frequently was 5–11, with the optimal pH for actinomycetes growth in the neutral region, especially 7. There were reports of actinomycetes capable of growing in a great range of NaCl, being 32% the maximum concentration of NaCl tolerance observed in the studies reviewed (Meklat et al. 2014). The range with the highest frequency was from 0 to 5% of NaCl, with the concentration of 0 to 1% being the most common tolerance reported as optimal for the growth of different species of actinomycetes.

Only < 2% of bacteria are culturable using common cultivation methods (Sedeek et al. 2022). Therefore, some procedures (pretreatments) are applied to perform better isolation of actinomycetes from soils (Meliani et al. 2022). Initially, soil samples are commonly dried at room temperature, in addition to the use of inhibitors to facilitate the isolation of these microorganisms. Cycloheximide (a fungicide generally used at a concentration of 50 mg/L) and nalidixic acid (a product with activity against Gram-negative bacteria usually used at a concentration of 20 mg/L) are the main inhibitors utilized for the isolation of actinomycetes. Besides, it was also observed the use of some pretreatments before the serial dilution step, such as thermal, microwaves, and sonication (Hozzein et al. 2019; Intra et al. 2019; Jin et al. 2018; Malek et al. 2015; Zahir et al. 2016). The isolation step carried out following certain combinations of procedures can obtain new strains of actinomycetes, which can produce new and unusual secondary metabolites with application in different industrial sectors (Ezeobiora et al. 2022). Figure 1 presents the required steps to isolate soil actinomycetes according to most of the articles analyzed.

Fig. 1.

Methodological steps commonly used for the isolation and cultivation of soil actinomycetes

The rhizospheric fraction (generally from 0 to 20 cm of soil depth) is the most explored region for isolation of actinomycetes (Fig. 1). As for the types of soil, a wide diversity was verified, such as soils from forests, mountains, mounts, agricultural areas, urban zones, contaminated areas, arid and semi-arid zones, saline soils, lake edges, muddy soils, among others. The isolation of actinomycetes from extreme environments, such as deserts (especially the Sahara), deep-sea sediments and Antarctica, has been the focus of different works to further explore their adaptive capabilities for different applications (Encheva et al. 2013; Fu et al. 2022; Meklat et al. 2013a, 2013b; Meliani et al. 2022; Rodríguez et al. 2018; Su et al. 2022; Xu et al. 2014).

The interest in isolating actinomycetes from the soil and exploring their potential applications has been the objective of several researchers around the world. Regarding the focus of the analyzed articles, most of the works carried out the isolation and description of new species of actinomycetes (± 40%), followed by the antimicrobial potential of actinomycetes (± 30%). The description of bioactive compounds with anticancer and antioxidant potential, enzymes production and agricultural uses also stood out among the focus of studies on soil actinomycetes applications. The use of soil actinomycetes on bioremediation, pigment production, ways to increase their population in the soil, and even the influence of contaminants on the growth of these microorganisms have been also carried out (Fig. 2). These potential applications are presented in detail in the subsequent items.

Fig. 2.

Growth capacity (temperature, pH, and NaCl tolerance) and main applications of soil actinomycetes according to 264 systematically reviewed articles from 2011 to 2022

Pharmaceutical uses of the actinomycetes

Actinomycetes are recognized for their antimicrobial potential, responsible for the production of about half of the bioactive compounds with antagonistic activity against different pathogenic microorganisms(Daquioag and Penuliar 2021; Devi et al. 2022; Sarika et al. 2021; Sarkar and Suthindhiran 2022). These antimicrobial compounds have high commercial value and have been applied in several areas, such as the food, agricultural, medical, pharmaceutical, and other industries (Alqahtani et al. 2022; Bizuye et al. 2013; Daquioag and Penuliar 2021; Devi et al. 2022; Sarika et al. 2021). The scientific community and public–private partnerships have been encouraged to discover new sources of antimicrobial agents and develop new products for pathogen control (Alqahtani et al. 2022). Table 1 presents several studies that addressed the antimicrobial potential of actinomycetes.

Table 1.

Antimicrobial potential of soil actinomycetes

Actinomycete	Observed inhibition (zone of inhibition: mm or inhibition rate: %)	Minimum inhibitory concentration (µg/mL)	Reference
Saccharothrix longispora	A. flavus (22.7 mm) and F. oxysporum (23.8 mm)	-	Meliani et al. (2022)
Actinomadura hibisca	A. flavus (15 mm)	-
Streptomyces vellosus	E. coli (15.65 mm)	-	Fatimah et al. (2022)
Streptomyces sp.	E. coli (22 mm), P. aeruginosa (22 mm), K. pneumoniae (22 mm), A. baumannii (18 mm), S. aureus (22 mm), E. faecalis (30 mm)	-	Liu et al. (2022)
Streptomyces sp.	C. albicans (21 mm), C. tropicalis (20.5 mm), S. cerevisiae (21 mm), B. subtilis (20 mm), E. faecalis (17.5 mm), P. aeruginosa (13.5 mm), S. typhi (11.5 mm)	C. albicans (125 to 500), C. tropicalis (31.25 to 500), S. cerevisiae (125 to 500), B. subtilis (250), K. pneumoniae (500), S. aureus (250), S. mutans (250 to 500)	Daquioag and Penuliar (2021)
Streptomyces sp.	B. subtilis (12 mm), B. cereus (9 mm), S. aureus (11.9 mm), S. pneumonia (18 mm), M. luteus (11 mm), E coli (12.1 mm), E aerogenes (10 mm), K. pneumoniae (11 mm), S. paratyphi (18 mm), P. aeruginosa (12 mm), C. albicans (16 mm)	-	Sarika et al. (2021)
Streptomyces sp.	E. coli (13 mm), S. aureus (18 mm), K. pneumoniae (4 mm), Bacillus sp. (2 mm), P. aeruginosa (3 mm)	-	Shrestha et al. (2021)
Micromonospora sp.	E. coli (12 mm), S. aureus (4 mm), K. pneumoniae (12 mm), Bacillus sp. (1 mm), P. aeruginosa (2 mm)	-
Nocardia sp.	E. coli (4 mm), S. aureus (18 mm), K. pneumoniae (10 mm), Bacillus sp. (2 mm), P. aeruginosa (1 mm)	-
Streptomyces sp.	S. aureus (20 mm), E. coli (18 mm), K. pneumoniae (16 mm)	-	Sapkota et al. (2020)
Micromonospora sp.	S. aureus (17 mm), E. coli (25 mm), K. pneumoniae (18 mm)
Nocardia sp.	S. aureus (20 mm), E. coli (16 mm), K. pneumoniae (11 mm)
Streptomyces oligocarbophilus	P. fluorescens (37 mm), Streptococcus sp. (30 mm), F. oxysporum (19 mm), Trichoderma sp. (24 mm)	-	Shirokikh and Shirokikh (2019)
Streptomyces sp.	S. albus (35 mm), S. aureus (33 mm), S. pyogenes (35 mm), E. coli (33.5 mm), K. pneumoniae (39.2 mm), P. aeruginosa (33 mm), S. typhi (30.5 mm), A. hydrophila (33.7 mm)	-	Jassaim and Jarallah (2019)
Streptomyces sp.	A. arborescens (34 mm), A. tenuissima (44 mm), A. niger (40 mm), B. cinerea (38 mm), F. poae (30 mm), P. expansum (34 mm), R. solani (9 to 37 mm), S. sclerotiorum (9 to 45 mm)	-	Javoreková et al. (2019)
Streptomyces sp.	E. coli (14.6 mm), A. niger (19.7 mm)	E. coli (94), S. aureus (125), B. subtilis (280), A. niger (125), C. albicans (250)	Retnowati et al. (2018)
Spirillospora tritici	B. berengeriana (16.3%), V. dahliae (11.5%), F. graminearum (10.6%), C. cucumerinum (14.8%)	-	Song et al. (2018)
Streptomyces sp.	Alternaria (13 mm), Botrytis (15 mm), Fusarium (8.5 mm), Phoma (14 mm)	-	Rodríguez et al. (2018)
Streptomyces sp.	A. caviae (13 mm), E. tarda (16 mm), V. harveyi (13 mm), V. anguillarum (17 mm)	-	Nabila and Kannabiran (2018)
Streptomyces indiaensis	R. oryzae (17 mm), U. maydis (19 mm), M. hiemalis (15 mm), F. moniliformis (16 mm), F. oxysporum (36 mm), A. fumigatus (25 mm), A. flavus (23 mm), A. niger (23 mm), A. solani (17 mm), H. graminum (22 mm)	R. oryzae (40), U. maydis (40), M. hiemalis (30), F. oxysporum (20), A. fumigatus (30), A. flavus (30), A. niger (30), A. solani (40), H. graminum (40)	Bhosale and Kadam (2018)
Nocardia alba	E. coli (11 mm), E. Faecalis (6 mm), K. pneumoniae (1 mm), M. luteus (2 mm)	E. coli (510), K. pneumoniae (510), E. faecalis (1020), M. luteus (1020)	Salim et al. (2017)
Streptomyces sp.	B. subtilis (42 mm), M. luteus (34 mm), S. aureus (36 mm), M. smegmatis (29 mm), E. coli (20 mm), P. aeruginosa (17 mm), C. violaceum (22 mm), C. albicans (10 to 14 mm), P. anomala (18 mm), M. hiemalis (18 mm)	-	Charousová et al., 2017
Streptomyces gamaensis sp. nov	S. sclerotiorum (62.3%), C. cassiicola (40.1%), C. lunata (23.1%), S. turcicaf (56.3%), H. maydis (29.2%), S. reiliana (23%), T. cucumeris (33%), F. oxysporum (33.2%), C. orbiculare (56.9%)	-	Zhao et al. (2017)
Streptomyces songpinggouensis	S. sclerotiorum (12%), C. cassiicola (12.3%), C. lunata (10.3%), H. maydis (11%), P. infestans (16.1%)	-	Guan et al. (2016)
Nocardia sp.	S. aureus (36 mm), S. epidermidis (23 mm), B. subtilis (28 mm), B. cereus (22 mm), B. megaterium (26 mm), M. luteus (22 mm), E. coli (31 mm), S. marcescens (18 mm), K. pneumoniae (15 to 27 mm), P. aeruginosa (26 mm), P. vulgaris (17 mm), C. albicans (27 mm), C. tropicalis (23 mm)	S. aureus (> 0,975 and > 1,95), S. epidermidis (> 7,81), B. subtilis (> 1,95), B. cereus (> 7,81), B. megaterium (> 3,9), M. luteus (> 7,81), E. coli (> 3,9), S. marcescens (> 31,2), K. pneumoniae (> 1,95), P. aeruginosa (> 1,95), P. vulgaris (> 31,25), C. albicans (> 1,95), C. tropicalis (> 7,81)	Sharma et al. (2016)
Streptomyces sp.	S. aureus (23 mm), P. aeruginosa (18 mm), E. coli (15 mm), S. typhi (13 mm), E. faecalis (12 mm), K. pneumoniae (16 mm), M. luteus (25 mm)	-	Ahmad et al. (2013)
Streptomyces sp.	B. subtilis (37 mm), X. euvesicatoria (20 mm), S. aureus (24 mm), S. epidermidis (23 mm), B. gladioli (31 mm), Pseudomonas sp. (20 mm), E. amylovora (15 mm)	-	Encheva et al. (2013)
Pseudonocardia sp.	S. aureus (> 20 mm), B. subtilis (10 mm), B. pasteurii (20 mm)	-	Jafari et al. (2014)
Streptomyces enissocaesilis	B. subtilis (23.3 mm), S. aureus (21 mm), E. coli (16.7 mm), S. marcescens (19.7 mm) C. albicans (17.7 mm)	-	Malek et al. (2015)
Streptomyces sp.	X. oryzae pv. oryzae (18.5 mm), X. oryzae pv. oryzicola (17.8 mm)	-	Muangham et al. (2015)
Streptomyces sp.	A. niger, Penicillium sp., B. subtilis: total inhibition; Fusarium sp., B. cereus, E. coli: inhibition	-	Kulkarni et al. (2012)
Nocardiopsis sp.	M. rammanianus (20 mm), A. niger (17 mm), P. expansum (18 mm), P. glabrum (17 mm), B. subtillis (22 mm), M. luteus (23 mm), L. monocytogenes (24 mm)	-	Meklat et al. (2011)
Streptomonospora sp.	M. rammanianus (15 mm), P. expansum (15 mm), M. luteus (15 mm)	-
Actinopolyspora sp.	M. rammanianus (17 mm), B. subtillis (15 mm), S. aureus (25 mm), K. pneumoniae (36 mm), L. monocytogenes (36 mm)	-
Saccharopolyspora sp.	M. rammanianus (13 mm), M. luteus (15 mm), L. monocytogenes (15 mm)	-
Kocuria kristinae	B. subtilis (< 5 mm), C. albicans (< 5 mm), S. marcescens (> 15 mm)	-	Bundale et al. (2018)
Actinomyces sp.	B. subtilis (< 5 mm), C. albicans (15 mm)	-
Micromonosporaceae sp.	B. subtilis (> 15 mm), E. coli (15 mm), C. albicans (15 mm), S. marcescens (> 15 mm)	-
Actinomycetales bacterium	B. subtilis (15 mm), E. coli (15 mm), S. marcescens (15 mm)	-
Glutamicibacter arilaitensis	C. albicans (15 mm)	-
Micromonospora auratinigra	B. subtilis (< 5 mm), E. coli (< 5 mm), C. albicans (< 5 mm), S. marcescens (15 mm)	-
Streptomyces werraensis	B. cereus (35 mm), S. aureus (38 mm), P. aeruginosa (19 mm), E. coli (40 mm), S. typhi (22 mm)	-	Devi et al. (2013)
Micromonospora sp.	P. aeruginosa (11 mm), S. aureus (12 mm)	-	Hamedi et al. (2015b)
Nocardia sp.	P. aeruginosa (18 mm), S. aureus (19 mm), A. niger (14 mm)	-
Streptomyces sp.	F. oxysporum f.sp. Dianthi (20 mm), F. oxysporum (18 mm), C. acutatum (29 mm), A. brassicicola (28.3 mm), R. Oryza f.sp. Sativae (14 mm), Cercospora sp. (19.3 mm), Exserohilum sp. (32 mm)	-	Kaur et al. (2013)
Streptomyces sp.	E. coli (20 mm), S. aureus (30 mm), S. viridochromogenes (20 mm), B. subtilis (120 mm), M. miehei (> 30 mm), C. albicans (30 mm), C. vulgaris (20 mm), S. subspicatus (20 mm), P. ultimum (30 mm), R. solani (20 mm), A. cochlioides (30 mm)	-	Ruanpanun et al. (2012)
Thermoactinomyces sp.	F. solani (20 mm), F. oxysporum (20 mm), A. niger (12 mm), Mucor sp. (20 mm)	-	Gousterova et al. (2011)

Among all the articles analyzed, 80 documents addressed the potential of actinomycetes to act as antimicrobial control agents. Streptomyces was the main genus of actinomycetes studied as an antimicrobial agent, with 42 (70.77%) mentions among the articles. Nocardia and Micromonospora were cited 6 (8.45%) times each. According to Sapkota et al. (2020), Streptomyces has a greater capacity to produce antibiotics, followed by Nocardia and Micromonospora. Bérdy (2005) reported the number of actinomycetes species that produce bioactive microbial metabolites, with approximately 8000 from the genus Streptomyces, 740 from Micromonospora and 357 from Nocardia.

Species of the genus Streptomyces are responsible producing about 75% of the bioactive microbial metabolites of all actinomycetes, with antimicrobial compounds as the main ones (Bérdy 2005; Sebak et al. 2019). Micromonospora and Nocardia are considered rare actinomycetes genera, given the difficulty of isolation and the need for different conditions to maintain them. These genera are recognized for their high potential to produce new bioactive compounds as a source of antimicrobial metabolites with different chemical structures (Talukdar et al. 2016).

New described species are also investigated as antimicrobial agents. Guan et al. (2016) used Streptomyces songpinggouensis to inhibit the fungi S. sclerotiorum, C. cassiicola, A. solani, C. lunata, S. turcicaf, H. maydis, F. oxysporum, C. orbiculare, and P. infestans, obtaining inhibition rates between 10 and 16%. Reddy et al. (2011) tested Streptomyces hyderabadensis sp. nov. for the inhibition of A. niger, A. flavus, F. oxysporum, E. coli, P. aeruginosa, S. aureus, and B. subtilis, being positive for all.

Therefore, actinomycetes are widely studied for antagonistic activity of several species of pathogenic microorganisms (Table 1). These studies mainly employed the agar-well diffusion method to verify antimicrobial potential. This method is one of the best known and most basic for the observation of antimicrobial activity, it consists of diffusing the antimicrobial extract in the well in agar medium with the target microorganism already inoculated (Balouiri et al. 2016). The solid media most used in antimicrobial assays were Mueller–Hinton agar and nutrient agar. In most studies, antimicrobial extracts were produced by submerged fermentation at 28 °C with agitation in the range of 110 to 200 rpm. The most used culture media were liquid ISP 2, starch and casein broth.

The conditions used in the inhibition assays generally depend on the target microorganism. For bacteria, most inhibitions assays were carried out for 24 h at 37 °C, and for fungi, they ranged from 48 to 72 h and the temperature from 25 to 30 °C. After incubation, antimicrobial potential can be determined by a reference standard, such as a positive control (if inhibition occurred) and/or by a zone or halo of growth inhibition (measurement referring to the distance from the circumference or well to the margin with the growth of the test microorganism) (Balouiri et al. 2016). Another factor evaluated in antimicrobial assays is the minimum inhibitory concentration (MIC), characterized by the lowest concentration of extract required to inhibit the growth of the target microorganism (Balouiri et al. 2016). Dilution methods are more appropriate for the measurement of MIC, commonly expressed in µg/mL or mg/L (Balouiri et al. 2016).

Different species of microorganisms have been used in antimicrobial tests, including bacteria, fungi, yeasts, and microalgae (Table 1). Bacteria are divided into Gram-positive and Gram-negative, being the most evaluated Gram-positive species Staphylococcus aureus and Bacillus subtilis, and Gram-negative Escherichia coli and Pseudomonas aeruginosa in the analyzed articles. In addition, the most mentioned fungi were Aspergillus niger and Fusarium oxysporum, while the yeasts were Candida albicans and Saccharomyces cerevisiae.

S. aureus, B. subtilis, and P. aeruginosa bacteria are pathogens that play a role in several infections with a high mortality rate (Talukdar et al. 2016). Staphylococcus aureus is responsible for causing infections of the skin, the central nervous system, bones and joints, skeletal muscles, respiratory, and urinary tract (Jafari et al. 2014; Talukdar et al. 2016). In addition, some strains of this bacterium are resistant to commonly used antibiotics (Jafari et al., 2014). Bacillus subtilis is the most frequent cause of urinary tract infections (Talukdar et al. 2016). B. subtilis is a microorganism of great importance for agriculture, as it participates in the biocontrol and nutrition of plants (Kovács 2019).

Pseudomonas aeruginosa is characterized by causing acute to chronic infections in immunocompromised people and patients with cystic fibrosis (Chevalier et al. 2017; Filho et al. 2013). A particularity is that its membrane has low permeability having high resistance to antiseptics and antibiotics (Chevalier et al. 2017). Escherichia coli is part of the intestinal microbiota, being generally harmless, however, they can cause infection if their host is weakened or immunosuppressed (Nataro and Kaper, 1998). Pathogenic strains are the causative agents of genetic diarrhea, mainly associated with outbreaks of childhood diarrhea (Nataro and Kaper 1998; Talukdar et al. 2016).

Darshit and Pandya (2019) studied the antimicrobial activity of actinomycete isolates against different bacteria, such as B. subtilis, S. aureus, P. vulgaris, E. coli, K. aerogenes, S. typhi, E. aerogenes, finding inhibition zones between 10 and 26 mm. Talukdar et al. (2016) studied the MIC of Micromonospora auratinigra for the inhibition of the growth of different bacteria, reaching a concentration of 70 µg/mL for S. aureus, 40 µg/mL for B. subtilis, 50 µg/mL for M. abscessus, 60 µg/mL for E. coli, and P. vulgaris, 80 µg/mL for P. aeruginosa. Besides, they reported for the first time the antimicrobial potential of M. auratinigra, identifying 2-methylfolepylisonicotinate, a natural analog of isoniazid (a broad-spectrum agent) as an antibiotic compound.

Candida albicans is a pathogenic yeast, responsible for most cases of fungal infections in humans, causing deep mycoses and vulvovaginal candidiasis (Zida et al. 2017). Aaron and Torsten (2020) report that C. albicans is an additional factor in the onset and course of celiac (autoimmune) disease, which affects the human small intestine. Saccharomyces cerevisiae is a yeast used in different sectors, such as food, biotechnology, and medicine, where it is known mainly as bread and beer yeast (Enache-Angoulvant and Hennequin 2005; Goebel et al. 2013; Pérez-Cantero et al. 2019). However, in recent years, it has been reported as a cause of fungemia in immunocompromised patients who use it for medicinal purposes (Enache-Angoulvant and Hennequin 2005; Goebel et al. 2013; Pérez-Cantero et al. 2019; Poncelet et al. 2021). Streptomyces sp. isolated from Iranian soils were evaluated against the antagonist activity of yeasts (C. albicans, S. cerevisiae) and a bacterium (E. coli) by Mehravar et al. (2011), who achieved zones of inhibition between 5 and 13 mm for C. albicans, 9 and 10 mm for S. cerevisiae, and 3 and 20 for E. coli.

Numerous antibiotic compounds can be extracted from actinomycetes, the best known and most important include tetracycline, streptomycin, neomycin, chloramphenicol, macrolide, erythromycin, rifamycin, vancomycin, gentamicin, kanamycin, and daptomycin (Bérdy 2005; Jose et al. 2021; Niu 2018; Oli et al. 2021; Shrestha et al. 2021). Over the years, many pathogens have become more resistant and tolerant to existing antibiotics, creating the need for strategies to discover new natural products (Ahmad et al. 2013; Chevalier et al. 2017; Lewis 2020; Niu 2018; Rutledge and Challis 2015). This fact aroused the interest of the scientific community to investigate new compounds and isolate promising actinomycetes species. In these studies, most of the metabolites identified with antimicrobial properties still did not have a description in the database, indicating promising new antibiotics (Retnowati et al. 2018; Sebak et al. 2019; Shrestha et al. 2021; Talukdar et al. 2016).

There are two attractive sources for obtaining new antibiotics from actinomycetes, which are: biosynthetic pathways of unexplored actinomycetes; uncharacterized biosynthetic pathways incorporated into the genome of cultured actinomycetes (Niu 2018). Actinomycetes stand out as a source of natural products due to their large genomes with clusters of biosynthetic genes (CBGs) capable of synthesizing different biocompounds (Niu 2018; Rutledge and Challis 2015). Natural products with antimicrobial action have some advantages over synthetic ones, such as acting against Gram-positive pathogens, not be limited by target type or mode of action and perform tasks that are difficult for synthetic products (Lewis 2020; Ye et al. 2020). In this way, it is possible to observe the distinction and importance of actinomycetes in the control of different pathogens, especially for those harmful to human health.

Actinomycetes can produce bioactive compounds with other pharmacological functions, such as antiviral, antitumor, antioxidant, anti-inflammatory, immunosuppressive, antiparasitic, and cytotoxic (Jose et al. 2021; Oli et al. 2021; Ruwandeepika et al. 2022). Several compounds derived from this bacterium are widely used clinically, such as anticancer drugs, which include anthracyclines, bleomycin, mitosanes, enediynes, and others (Jose et al. 2021; Oli et al. 2021; Ruwandeepika et al. 2022). Anthracyclines derivatives (erythromycin, doxorubicin, and epirubicin) are used to treat various types of cancer (Chen et al. 2018a; Lu et al. 2017). Cancer is one of the major causes of morbidity and mortality worldwide, so these compounds are essential, indicating advances in science and instigating the constant search for new drugs (Assad et al., 2021; Chen et al. 2018a; Lu et al. 2017; Osama et al. 2022).

Studies have already been reported with actinomycetes to combat different viruses that affect human health, such as hepatitis C virus (HCV), influenza A virus (IAV), human immunodeficiency virus (HIV), herpes simplex virus (HSV), and epidemic diarrhea virus (EDV). Compounds identified as antiviral agents were labyrinthine, chartreusin for HCV, xiamycin, butanolides, and antimycins (Berezin et. 2019; Chen et al. 2018b; Li et al. 2020; Padilla et al. 2015; Ruwandeepika et al. 2022). In addition, actinomycetes also show effects against parasitic diseases caused by Leishmania sp., Trypanosoma sp. (Chagas) and helminths, having as agents valinomycin, butanolides, avermectins, and milbemycins (Cheng et al. 2015; Jose et al. 2021; Ruwandeepika et al. 2022) Several parasitic compounds have been studied against Plasmodium sp. (cause of malaria), such as naseseazine, lorneic acid, octaminomycins, opantimycin, polycyclic xanthone, and gancidin (Jose et al. 2021; Ruwandeepika et al. 2022; Zin et al. 2017).

Bioactive compounds such as hexaricins, polyketides, pyrazolofluostatins, and agelolines showed antioxidant activities, protecting against various infections and degenerative diseases associated with reactive oxygen species (Gao et al. 2018; Jose et al. 2021). Other varieties of bioactive compounds change the immune response in humans, such as therapeutic immunosuppressants or drug immunoconjugates. Rapamycin, tacrolimus, and sirolimus are known compounds for this purpose (Jose et al. 2021; Ruwandeepika et al. 2022). The anti-inflammatory activities are due to compounds such as trienomycins, butenolides, actinoquinolines, herbidosporadalins, and amycolataiwanensins (Chen et al. 2022; Gao et al. 2022; Jose et al. 2021; Su et al. 2021). These distinct properties of bioactive compounds derived from actinomycetes demonstrate the importance of this microorganism for pharmaceutical use.

Applications in food and other industries

Enzymes are biocatalysts produced by organisms in their cells to regulate the physiological process of living beings (Salahuddin et al. 2011), but mainly by microorganisms when the application is industrial (Abdallah et al. 2012; Ovais et al. 2018; Salahuddin et al. 2011). Enzymes from microbial sources are generally regarded as safe, stable, and functional at a wide range of temperature, pH, and salinity (Mukhtar et al. 2017; Sarkar and Suthindhiran 2022). Actinomycetes have ecological and biochemical diversity, high capacity to produce secondary metabolites, and can be considered an excellent source of enzymes with new specificities and applications (Benhadj et al. 2019; Ezeobiora et al. 2022; Gunjal and Bhagat 2022; Mukhtar et al. 2017; Sarkar and Suthindhiran 2022). Enzymes have been used in several industrial sectors, including the food industry (Sarkar and Suthindhiran 2022). Table 2 presents a series of studies about the production of enzymes from different species of actinomycetes.

Table 2.

Enzymes production from different species of actinomycetes

Actinomycete	Enzyme(s)	Experimental conditions		Enzymatic activity	Application	Reference
		pH	Temperature
Streptomyces avermitilis	Lytic polysaccharide monooxygenase	6.0	25–27 °C	0.019 ± 0.001 U mL−1	Biodegradation of lignocellulose	Utarti et al. (2021)
Microbispora cellulosiformans	Cellulase	NS	NS	+	Cellulose degradation	Gong et al. (2020)
Streptomyces strains	Chitinase	NS	NS	+	Control of parasite fruit fly larvae and pupae	Suryaminarsih et al. (2020)
Streptomyces	Cellulase	7.0	35 °C-30°C	+	Cellulose degradation	Nauanova et al. (2018)
Streptomyces thermoalkaliphilus	Cellulase	9.0	50 °C	19.5 ± 1.5 IU mL−1	Degradation of carboxymethylcellulose	Wu et al. (2018)
Streptomycetaceae, Pseudonocardiaceae, Micromonosporaceae and Promicromonosporaceae	Endocellulase, Xylanase, Pectinase, and Chitinase	NS	40 °C	+	Degradation of complex polysaccharides	Yeager et al. (2017)
Amycolatopsis of family Pseudonocardiaceae	Chitinase, Protease, Glucanase, Lipase, and Amylase	NS	28 °C	+	NS	Sadeghian et al. (2016)
Streptomyces rimosus	Chitinases (N-acetylhexosaminidase, Exo-chitinase, Endo-chitinase)	8.0	40 °C	78.8; 10.8; 83.4 U mg−1 protein, respectively	Growth inhibition of fungal phytopathogens	Brzezinska et al. (2013)
NS	Phosphatase	NS	37 °C	+	Dephosphorylation of soil organic compounds	Ghorbani-Nasrabadi et al. (2013)
Streptomyces avermitilis and Streptomyces labedae	L-glutaminase	7.0–8.0	30 °C	8.41 e 12.23 U mL−1, respectively	NS	Abdallah et al. (2012)
Streptomyces	Chitinase, Protease, Cellulase, and Pectinase	NS	26 °C	+	Control of plant pathogens; Degradation of trophic proteins; Mineralization of dead plant mass; Biocontrol of fungal pathogens	Golińska and Dahm (2011)
Nonomuraea sp.	Inulin fructotransferase	5.5	65 °C	60.3 U mL−1	Production of di-D-fructofuranose 1,2′:2,3′ dianhydride	Pudjirahart et al. (2011)
Streptomyces, Amycolatopsis, and Nocardioides	CMCase, Xylanase, Amylase, Pectinase, Chitinase, and Protease	7.0	30 °C	+	Stabilization of the soil structure; Decomposition of organic waste; Formation of organic matter; Nutrient cycling	Sonia et al. (2011)

+ : positive for enzyme (s) production. NS: not specified

The genus of actinomycetes that was most evident in enzyme production studies was Streptomyces, which is responsible for the production of several enzymes, such as lytic polysaccharide monooxygenase, chitinases, proteases, cellulases, pectinases, L-glutaminase, CMCase, xylanases, and amylases. The most identified enzymes were chitinases and cellulases, and most of the selected studies verified the enzymatic activity of a given enzyme, while some studies quantified the activity (Table 2). In general, the test parameters analyzed were pH and temperature. Thus, it is evident that, for diverse applications, it is necessary to identify the temperature and pH conditions concerning the enzymatic activity.

Enzymes with heat stability have attracted interest due to their potential application in industrial sectors, as there is a reduction in the risks of contamination by common mesophiles at higher process temperatures (Sarkar and Suthindhiran 2022; Sonia et al. 2011). This increase in the temperature can also improve the efficiency of substrate degradation, as with higher temperature, the solubility of substrates and products tends to increase, while the viscosity of the medium decreases, allowing an increase in the substrate diffusion coefficient and, therefore, in the reaction rate (Kumar and Swati 2001; Sonia et al. 2011). In this context, by producing α-amylase from thermophilic actinomycetes, Salahuddin et al. (2011) verified that this enzyme showed higher activity and stability at 55 °C in using starch as a substrate. Regarding pH, α-amylase showed maximum activity at pH 6.0. For the authors, these results highlight that isolated actinomycetes can produce thermostable and extracellular enzymes, which have applicability in various industrial sectors. Therefore, actinomycetes can produce amylases used in different industries, especially in the food sector (Aguiar et al. 2022). Amylases can be applied in the conversion of starch into high-fructose syrups, while thermophilic amylases can be used in bakery, brewery, and alcohol industries (Prakash et al. 2013).

In addition to thermostable enzymes, it is important to emphasize chitinases and cellulases, since they were the enzymes that most stood out in Table 2. Wu et al. (2018) verified the capacity to produce alkaline cellulase from Streptomyces thermoalkaliphilus, obtaining an enzymatic activity of 19.5 ± 15 IU mL⁻¹. Therefore, this enzyme showed potential carboxymethyl cellulose degrading activity. Cellulases produced by actinomycetes can be applied for the bioconversion of plant-based cellulosic and lignocellulosic waste, representing an alternative to overcome this bottleneck in the food sector and environmental management (Swamy et al. 2022). On the other hand, chitinases are responsible for the biodegradation of chitin, being able to act in the growth inhibition or control of plant pathogens, especially insects (Golińska and Dahm 2011; Suryaminarsih et al. 2020). Streptomyces strains present high potential for chitinolytic enzyme production (Duhsaki et al. 2022; Singh and Gaur 2016).

Other enzymes, such as proteases, pectinases, xylanases, glucanases, among others, were also produced from actinomycetes in the selected studies. In addition, authors report the capacity of actinomycetes for lipases and keratinases production (Maldonado et al. 2022; Pizarro et al. 2022). Lipases catalyze the hydrolysis of lipids such as triacylglycerol in glycerol, with potential application in the processing of oils and fats, cosmetics, and detergents (Mukhtar et al. 2017; Pizarro et al. 2022; Salgado et al. 2022). Keratinases act in the hydrolysis of keratin and can be used to recycle waste such as chicken feathers and nails, converting them into products of commercial value (Mukhtar et al. 2017). Keratinases can also be used in other areas such as agriculture, textiles, and cosmetics (Maldonado et al. 2022). Golińska and Dahm (2011) identified the presence of protease and pectinase activity, with potential application in the degradation of trophic proteins and the mineralization of dead plant mass, respectively. Streptomyces, Nocardia, and Nocardiopsis have been reported as producer of proteases (Gopal et al. 2022). In terms of industrial application, proteases have potential use in the food industry in the process of milk coagulation, clarification of fruit juices, degumming of fiber and winemaking, and also in the paper industry, acting in the removal of biofilm (Kirk et al. 2002; Li et al. 2012; Prakash et al. 2013). On the other hand, pectinases can be used in fruit-based foods and beverages, textile, paper and pulp industry, agriculture sector, and bioenergy production (Kirk et al. 2002; Li et al, 2012; Haneen et al. 2022). Actinomycetes are also pectinolytic microorganisms (Haneen et al. 2022). As a result of the application of many enzymes in the food industry, the use of catalase has been exploited in processes such as the production of cheese, as an antioxidant enzyme system with glucose oxidase, in the removal of glucose from egg whites, in food wrappers and in checking milk quality (Kaushal et al. 2018). The transglutaminase enzyme has also been used in the food industry in meat and dairy products, such as low-fat yogurts (Miwa 2020).

Sonia et al. (2011) stated that xylanases play an important role in stabilizing soil structure and decomposing organic waste. Industrially, xylanases can be applied in the production of animal feed, as agents that facilitate digestion, as well as glucanases, which can also be used in the mashing process (Kirk et al. 2002; Li et al. 2012). Furthermore, Yeager et al. (2017) evaluated the activity of endocellulase, xylanase, pectinase, and chitinase in the degradation of complex polysaccharides. Xylanase activity was the most common, being produced from 73 isolates out of a total of 392, followed by pectinase, produced from 40 isolates. In both cases, most of the isolates belonged to the Streptomycetaceae family. Thus, the potential use of actinomycetes in enzyme production is evident, as they can produce a variety of enzymes with applications in different areas of interest.

Enzymes have numerous advantages over chemical agents, as the reactions occur under milder conditions of pH and temperature, and the products obtained preserve their properties, however, there are still limitations in some sectors (Miwa 2020; Saqib et al. 2017). In the food industry, free enzymes used in a soluble form present challenges related to low operational stability and high cost (Xavier et al. 2019). Furthermore, the use of free enzymes difficult the reuse process (Ricardi et al. 2018). The immobilization process has advantages compared to the enzyme in its free form such as operational stability, possibility of recovery of the biocatalyst, implementation in continuous processes, cost reduction, and absence of the biocatalyst in the final product (Damin et al. 2021, Datta el al. 2013; Harir et al. 2017; Salgado et al. 2022). This process can occur through adsorption, covalent bonding, confinement, cross-linking, and ionic bonding (Damin et al. 2021). Among the proposed methods for enzyme immobilization, adsorption is the most used (Jesionowski et al. 2014; Reis et al. 2019). Several compounds can be used as enzyme carriers. The most common inorganic carriers are silicas, titania, and hydroxyapatite, while organic carriers include chitin, chitosan, cellulose, alginate, as well as synthetic polymers (Jesionowski et al. 2014). In the studies realized by Afzali et al. (2021), the strain identified as Streptomyces griseobruneus, capable of producing the extracellular enzyme cyclodextrin glucanotransferase, was immobilized in different compounds. The results show that the enzymatic activity was 1109, 948, and 606 U mL⁻¹ in alginate/chitosan/microcrystalline cellulose (MCC) sheets, agar/gelatin/MCC beads, and free cells, respectively. Therefore, it is possible to observe that the polymeric immobilization was effective in improving the production of enzymes, due to the properties of the composites such as the protection against inhibitors and toxins. Harir et al. (2017) isolated the enzyme tyrosinase from extremophile bacteria and immobilized it in nylon nanofiber membranes. The immobilization efficiency was 82% when the enzyme concentration was 1 mg mL⁻¹ and with 1% of glutaraldehyde. The process increased the stability of the enzyme and facilitated its reuse. This enzyme can be applied in different biotechnological fields, like pharmaceutical, wastewater treatment, and food bioprocessing (Zaidi et al. 2014).

In this sense, actinomycetes can produce a variety of enzymes with potential applications in different industries. In the food industry, enzymes can improve the functional, nutritional, and sensory properties of products, with wide application in the processing of many food products. In addition, the importance of enzymatic technology is attracting attention to meet the diversifying food needs of consumers. However, it is necessary to use optimization approaches, where new techniques that allow better performance in enzymatic catalysis must be applied.

Agricultural uses

Actinomycetes have been studied to produce biofertilizers and biocontrol agents aiming the replacement of synthetic compounds to increase sustainability in agriculture (AbdElgawad et al. 2020; Bouizgarne 2022; Boukhatem et al., 2022; Djebaili et al. 2020; Farda et al. 2022; Javed et al. 2021; Meliani et al. 2022; Mitra et al. 2022; Soumare et al. 2021). Biofertilizers are products with microorganism free cells and, when applied to the soil, promote the release of nutrients to the soil and/or crops (Asadu et al. 2018, 2020). Biocontrol agents have been used to control plant diseases, which release secondary metabolites for the disease in question (Marin-Bruzos et al. 2021). Actinomycetes produce various high value-added secondary metabolites with agronomic potential (Boubekri et al. 2022; Fu et al. 2022; Mitra et al. 2022).

Due to the population increase and the high levels of poverty in the world, the literature presents several alternatives of secondary metabolites to control microorganisms and crop pests, in addition to the search to improve the quality of crops (AbdElgawad et al. 2020; Fu et al. 2022; Grubbs et al. 2021; Helal et al. 2016; Nauanova et al. 2018). Several bacteria and fungi are already widely applied to soils to replace agrochemicals, such as Bacillus sp. (Salwan et al. 2021; Schueler et al. 2021) and Trichoderma sp. (Sharma et al. 2022; Zin and Badaluddin 2020), but due to the abundance of actinomycetes and their resistance to temperature, pH and different potential applications, these microorganisms present great potential for agriculture uses (Bouizgarne 2022; Boukhatem et al. 2022; Farda et al. 2022; Meliani et al. 2022; Ruangwong et al. 2022; Sarkar and Suthindhiran et al. 2022).

Actinomycetes collaborate with several beneficial properties for soil quality and plant growth, as they excrete enzymes, increase soil fertility, promote greater fixation of atmospheric nitrogen (N₂) and are also capable of promoting the recycling of organic matter, controlling pests and diseases, act as fatty acid methyl esters (FAME) biomarkers, and bioremediate soils (AbdElgawad et al. 2020; Bacmaga et al. 2015; Bouizgarne 2022; Boukhatem et al. 2022; Helal et al. 2016; Hozzein et al. 2019; Javed et al. 2021; Mahyarudin et al. 2015; Meliani et al. 2022; Poomthongdee et al. 2014; Rathore et al. 2022; Ruangwong et al. 2022). Table 3 presents some studies on actinomycetes in the agricultural context and their respective effects on the studied soils and crops.

Table 3.

Actinomycetes utilization in the agricultural context

Actinomycete	Growing conditions	Influences	Reference
Streptomyces sp.	28 °C for 2 d	Inhibited the mycelial growth of the fungus Phytophthora infestans that causes late blight in potato cultivation, being 11 of the secondary metabolites found as possible biocontrol agents	Fu et al. (2022)
Streptomyces sp.	28 °C for 14 d	Increased the amount of minerals, vitamins and antioxidants in the seeds, and increased the amount of N2 and nutrients in the soil	AbdElgawad et al. (2020)
Streptomyces sp. and Nocardiopsis sp.	30 °C for 7 d	High production of ammonia and indole acetic acid were obtained, and inorganic phosphate was dissolved	Djebaili et al. (2020)
Streptomyces sp.	NS	There was a production of chitinase and pest control	Suryaminarsih et al. (2020)
NS	27 °C, 7 to 14 d	Increased the quality of the cereal grain, improved the quality of the soil and there was antioxidants excretion	Hozzein et al. (2019)
NS	20 to 22 °C for 7 d	Some species promoted the quality of the crop	Nauanova et al. (2018)
NS	30 °C for 4 d	Potential to control nematodes	Helal et al. (2016)
Streptomyces malaysiensis	35 °C for 7 d	Antifungal potential for the fungus Phytophthora sp.	Khucharoenphaisan et al. (2016)
Streptomyces sp.	28 °C for 7 d	Had antifungal potential and promoted better crop quality	Sreevidya et al. (2016)
NS	28 ºC for 7 d	Herbicides caused the inhibition of urease and phosphatase enzymes	Bacmaga et al. (2015)
Streptomyces sp.	28 ºC for 7 d	Antimicrobial potential	Muangham et al. (2015)
NS	5 to 20 °C	Showed antimicrobial activity	Dubrova et al. (2013)
NS	28 °C for 14 d	Soil pH and salinity have no significant influence on Actinomycetes	Ghorbani-Nasrabadi et al. (2013)
NS	28 °C, 7 to 14 d	Presented antimicrobial potential and promoted the quality of the crop with the production of indole acetic acid, increased N2 fixation and production of enzymes	Kaur et al. (2013)
Streptomyces sp.	NS	All the isolates produced siderophore, and two novel isolates were found, a Streptomyces that excreted enterobactin and a Streptomyces putatively producer of heterobactin	Lee et al. (2012)
Streptomyces sp.	28 °C for 7 d	Effects on root-knot nematodes; degrades casein, resistant to penicillin, inhibits the growth of Gram-positive and -negative bacteria, yeasts, fungi, and algae	Ruanpanun et al. (2012)
Thermoactinomyces sp.	NS	Activity against phytopathogenic fungi and proteolytic and lipolytic activity, and there was an improvement in soil quality through the insertion of feather wastes, which had a positive effect on soil urease and microbial activity, seed germination, and ryegrass growth	Gousterova et al. (2011)

The most identified actinomycetes genus for agricultural uses was also Streptomyces, which present a growth temperature pattern as they are mesophilic microorganisms, with a temperature variation in the articles from 20 to 35 ºC, and with a growth time of 7 to 28 days (Table 3). In the soil, actinomycetes increase the fixation of nitrogen and phosphate solubilization, essential components for the good development of crops, besides excreting secondary metabolites such as antioxidants, antimicrobials, and enzymes (AbdElgawad et al. 2020; Bouizgarne 2022; Boukhatem et al. 2022; Hozzein et al. 2019; Kaur et al. 2013; Ruangwong et al. 2022). The increase in the quality of the final product of crops was also observed in several studies, as there was an increase in nutritional factors, micro and macronutrients, and phenolics in foods (AbdElgawad et al. 2020; Hozzein et al. 2019; Soumare et al. 2021). Another compound that was widely observed in studies was indoleacetic acid, capable of promoting plant growth, root elongation, cell division, and root proliferation (Djebaili et al. 2020; Kaur et al. 2013). These factors are important for the replacement of conventional practices in agriculture.

Bacmaga et al. (2015) studied the influence of three herbicides, which demonstrated that urease and phosphatase enzymes are sensitive to the compounds, however, their use boosted the multiplication of actinomycetes, as they possibly used the herbicides as a source of carbon and/or nutrients. Several studies analyze the capacity of actinomycetes against insects and crop pests. Helal et al. (2016) studied the ability of actinomycetes to control nematodes, which showed the production of metabolites with ovicidal and larvicidal activity against these pests, and Soliman et al. (2021) proved that Streptomyces was able to produce secondary metabolites against Galleria mellonella larvae. Khucharoenphaisan et al. (2016) found the antimicrobial activity of actinomycetes against the fungus Phytophthora sp. because there was the excretion of secondary metabolites, and the possible hypothesis of control of this fungus was related to the hydrolytic capacity of the chitinase enzyme. Therefore, actinomycetes are promising microorganisms to control several phytopathogens (Bouizgarne 2022; Meliani et al. 2022).

Pathogenic fungi mainly affect plants and foods, causing diseases such as rust, stains, and rot. These diseases cause serious complications in plantations, harming agriculture in different aspects (Bhosale et al. 2018; Fu et al. 2022; Javoreková et al. 2019). The fungus Aspergillus niger is the cause of black mold in vegetables, aspergillosis in animals and a food contaminant. Some strains produce a nephrotoxic mycotoxin (ochratoxin), which has teratogenic, immunosuppressive, and carcinogenic properties (Choudhury et al. 2010; Soares et al. 2013). Fusarium oxysporum is a fungus known to cause diseases in various vegetables, flowers and crops, such as tomatoes, melons, beans, bananas, cotton, chickpeas, among others. Diseases that induce wilt, penetrate roots and, when they invade the vascular system, cause tracheomycosis (Fravel et al. 2003; Michielse and Rep 2009).

Bhosale et al. (2018) isolated the actinomycete Streptomyces indiaensis and used it for antagonist activity against several fungi, reaching greater inhibitions for F. oxysporum, A. fumigatus, A. flavus, A. niger, and H. graminum, from 22 to 36 mm. In addition, they studied the MIC of these microorganisms, obtaining 20 µg/mL for F. oxysporum, 30 µg/mL for A. fumigatus, A. flavus, and A. niger, 40 µg/mL for H. graminum. The antifungal activity of Streptomyces is commonly related to the extracellular hydrolytic enzymes that produce (Daquioag and Penuliar 2021). In this sense, actinomycetes are effective for the prevention of pests that commonly affect different crops.

As presented by Grubbs et al. (2021), apiculture has also been looking for bioactive compounds from actinomycetes as an alternative to fight diseases in the bees and their cultures. Streptomyces were isolated from bee pollen reserves, from which they obtained piceamycin, a polyketide, substance that has an inhibitory activity on the microorganism Paenibacillus larvae, responsible for the American foulbrood disease in bee brood (Grubbs et al. 2021). Polyketide pesticides are already widely marketed and their results are effective (Li et al. 2021). Lee et al. (2012) evaluated the production of siderophore by actinomycetes, which are secondary metabolites excreted by non-ribosomal peptide synthetases when there are low iron concentrations in the medium. Siderophores are iron III chelating substances, to turn the iron ions available to the microorganisms, an important micronutrient (Lee et al., 2012). The most common classifications of siderophores are catechol and hydroxamate (Lee et al., 2012). In this way, the action and secondary metabolites produced by actinomycetes can prevent the diseases and pests that commonly affect different crops, thus increasing their productivity and soil quality.

Sreevidya et al. (2016) evaluated the influence of Streptomyces sp. on the quality of chickpea cultivation, in which the insertion of the actinomycete increased the root and number of seeds by 17% and 22%, respectively, compared to the control, among many other positive points. The rhizospheric soil cultivated with chickpea and Streptomyces sp. obtained an increase of 11% in total nitrogen and 27% in available phosphorus. With these results, Sreevidya et al. (2016) prove that there was a production of enzymes for the conversion of unavailable to available phosphate, and there was also the production of lytic enzymes, which convert complex molecules into simpler and bioavailable molecules. AbdElgawad et al. (2020) obtained promising results in the soil quality by inoculating with actinomycetes since an increase in the amount of minerals, total phenolics, organic matter, and nitrogen was observed. In the evaluation of the nutritional quality of the legumes, there was an increase in the vitamins, antioxidants, and essential and non-essential minerals in the seeds (AbdElgawad et al. 2020). Therefore, actinomycetes present positive impacts on soil and plant quality, and in the control of pathogens and pests, representing an environmental-friendly alternative for agriculture.

Environmental purposes and other uses

Actinomycetes are one of the predominant microorganisms in soils, being responsible for many decomposition processes (Al-Maliki et al. 2021). They have metabolic diversity and specific growth characteristics, being resistant to extreme soil conditions and stimulating plant growth (Olajuyigbe and Ehiosun 2016; Polti et al. 2011). Furthermore, they have applications in areas such as medicine (Daquioag and Penuliar 2021), agriculture (Gong et al. 2020), cosmetic production (Dahal et al. 2017a), dyes (Kheiralla et al. 2016), bioremediation (Khedkar and Shanker 2014), among others. Table 4 presents different potential applications of actinomycetes, such as an agent capable of bioremediating several compounds, biodiesel production, antimalarial activity, carbon mineralization, and cosmetology.

Table 4.

Environmental applications of soil actinomycetes

Actinomycete	Application	Main results	Reference
Streptomyces coelicolor	Bioethanol production	- The highest ethanol yield of the strain was after 21 days of incubation, being 43.08 g L−1	Buraimoh et al. (2021)
Rhodococcus qingshengii	Carbendazim bioremediation	- 93% of carbendazim was removed from the soil after 14 days of incubation - Members of the genera Arthrobacter, Bacillus, Brevundimonas, Lysinibacillus, Massilia, Mycobacterium, Paenibacillus, and Pseudarthrobacter might be participated in the degradation process	Chuang et al. (2021)
Gordonia amicalis	Biodegradation of diesel oil	- G. amicalis HS-11 degraded 92.85% of diesel oil in 16 days of aerobic incubation - It synthesized active compounds from the surface extracellularly, reducing surface tension from 69 to 30 mN m−1 after 16 d	Sowani et al. (2020)
Calidifontibacter terrae	Cosmetics	- Enzyme inhibitory and antibacterial activities that may have application in the manufacture of cosmetics	Dahal et al. (2017a)
Actinokineospora acnipugnans	Cosmetics	- Activity against Propionibacterium acnes and Staphylococcus epidermidis - The strain showed anti-tyrosinase, anti-aging, and antioxidant activity	Dahal et al. (2017b)
Streptomyces coelicolor	Biodiesel production	-The most potent lipid producer was identified as Streptomyces coelicolor - 93% of the fatty acids from Streptomyces were converted to the corresponding fatty acid methyl esters	El-Sheekh et al. (2017)
Not specified	Antimalarial activity	- The crude acetone extracts of H11809 and FH025 showed inhibition on the growth of Plasmodium falciparum in vitro with 50% inhibitory concentration values of 0.57 and 1.28 μg mL−1, respectively - Dibutyl phthalate was, in part, the bioactive component that contributed to the antimalarial activity	Dahari et al. (2016)
Kineosporia, Mycobacterium and Micromonosporaceae	Cyanide bioremediation	- Actinomycetes outperformed other microorganisms to use ferrocyanide as a carbon source	Gschwendtner et al. (2016)
Streptomyces torulosus	Natural dyes	- The isolate produced reddish and greenish black pigments - Positive for melanin pigment production, nitrate reduction test, starch hydrolysis - Capable of producing H2S by fermentation and degrading xanthine, L-tyrosine and casein	Kheiralla et al. (2016)
Streptomyces, Saccharothrix, Streptosporangium, Promicromonospora, and Nonomuraea	Heavy metal bioremediation	- Some strains showed resistance to ZnCl2, CuSO4, CdCl2, and NiCl2 - Promicromonospora sp. UTMC 2243 was able to reduce 96.5% of the residual cadmium concentration	Hamedi et al. (2015a)
Rhodococcus erythropolis	Sulfur bioremediation	- 85% transformation of dibenzothiophene (270 μmol l−1) in 4 days - The isolate removed sulfur from the dibenzothiophene producing 2-hydroxybiphenyl and sulfate - The isolate exhibited susceptibility to lysozyme, resistance to penicillin and mitomycin C	Khedkar and Shanker (2014)
Microbacterium sp.	Anthracene biodegradation	- The isolate exhibited growth rate and doubling time of 0.82 d−1 and 0.84 d, respectively, in anthracene - Anthracene degradation 57.5 and 90.1% in 12 and 21 days, respectively, while the rate of anthracene utilization by the isolate was 4.79 mg L−1 d−1	Salam et al. (2013)

One of the applications that stood out among the analyzed studies was the use of actinomycetes for soil bioremediation through the bioaugmentation technique. Bioremediation is of interest as it presents environmental compatibility, low cost, and economic benefits (Cheng et al. 2022). Bioaugmentation consists in the use of microorganisms, native or cultivated, to reduce, remove or transform contaminants present in the soil (Aparicio et al. 2018a, 2018b; Costa-Gutierrez et al. 2021). Contaminated areas naturally present microorganisms with the ability to degrade a wide range of contaminants, but many contaminants are resistant to biodegradation due to factors such as low water solubility, low bioavailability, high toxicity, and high stability (Mawang et al. 2021). Thus, actinomycetes can be applied in bioremediation processes, as they have a ubiquitous distribution in aquatic and terrestrial ecosystems and tolerate extreme conditions (Aparicio et al. 2018a; Mawang et al. 2021; Sarkar and Suthindhiran 2022). Furthermore, they are responsible for the production of extracellular enzymes that degrade several complex organic compounds, production of spores that are impervious to desiccation and filamentous growth that favors the colonization of soil particles, acting as suitable agents for the bioremediation of metals and organic compounds in polluted soils (Salam et al. 2013; Timková et al. 2018).

Strains isolated from Iran soils were analyzed by Hamedi et al. (2015a), aiming the bioremediation of soils containing heavy metals. The results showed that some strains exhibited resistance to ZnCl₂, CuSO₄, CdCl₂, and NiCl_2. Furthermore, when studied the removal of cadmium by Promicromonospora sp. UTMC 2243, there was a reduction of 96.5% in the residual concentration of the metal, showing the ability of the actinomycete to remove this inorganic contaminant. It is known that non-essential heavy metals such as mercury, arsenic and cadmium do not present any biological benefit, being considered toxic to the ecosystem (Srivastava and Majumder, 2008). Thus, in addition to tolerating high concentrations of heavy metals, actinomycetes can remove or stabilize metals in less toxic or non-toxic substances and, consequently, reduce the bioavailability of these substances to other organisms (Aparicio et al. 2018a; Hamedi et al. 2015a). Actinomycetes of the genus Streptomyces, Nocardia, and Rhodococcus also exhibited resistance to heavy metals (Mawang et al. 2021).

Other contaminants that have caused great concern are pesticide residues in agricultural products, as well as their disposal in the environment. Chuang et al. (2021) studied the bioremediation of the fungicide carbendazim by the actinomycete Rhodococcus qingshengii. The strain showed potential for bioremediation of soils contaminated with carbendazim, with 93% of carbendazim removal from soils after 14 days of incubation. Gschwendtner et al. (2016) reported that actinomycetes overcome other microorganisms to use ferrocyanide as a carbon source in a cyanide bioremediation context. Cyanide is produced by several organisms as a defense mechanism, however, through the formation of very stable metal-cyanide complexes, they limit the nutrients present in the environment, making them unavailable to the organisms (Gschwendtner et al. 2016). Therefore, the bioremediation of cyanide present in soils is fundamental to ecosystems.

Khedkar and Shanker (2014) isolated a strain of soil contaminated with crude oil and evaluated its desulfurization property. The isolate Rhodococcus erythropolis showed 85% transformation of dibenzothiophene (270 μmol L⁻¹) in 4 days. Sulfur is present in fossil fuels, with the content in crude oil ranging from 1000 to 3000 ppm (Das et al. 2020; Khedkar and Shanker 2014). During the combustion reaction, sulfur is released as harmful sulfur oxides into the atmosphere, thus it is evident the need for desulfurization of crude oil for later use in the production of other fuels (Khedkar and Shanker 2014). Anthracene is also a contaminant regularly found in oil-polluted places, being considered recalcitrant because of the low water solubility and the high aromaticity compared to phenanthrene or pyrene (Garcia-Cruz and Martinez-Magadan 2007). Salam et al. (2013) evaluated the biodegradation of anthracene through an actinomycete strain, which degraded 57.5 and 90.1% of anthracene in 12 and 21 days, respectively. In addition to the pollutants mentioned above, actinomycetes are capable to bioremediate oils (Bhatti et al. 2017), herbicides (Castillo et al. 2006), insecticides (Abraham and Gajendiran 2019), organochlorines (Fuentes et al. 2010), and hydrocarbons present in petroleum (Chandraja et al. 2014).

Secondary metabolites can also be used as alternatives in the development of new products. In the study of Kheiralla et al. (2016), pigments were developed from rhizospheric actinomycetes, in reddish and greenish black colors, and their application was tested in wool and polyamide dyeing. Pigments from microbial sources such as natural dyes are alternatives that aim to generate less environmental impact than synthetic pigments (Kheiralla et al. 2016). Dahal et al. (2017b) reported the potential application of Actinokineospora acnipugnans in cosmetics, since the strain showed anti-aging and antioxidant activity. Furthermore, Dahal et al. (2017a) evidenced enzyme inhibitory and antibacterial activities of the actinomycete Calidifontibacter terrae, which have potential application in the manufacture of cosmetics.

Another application of actinomycetes that has been highlighted is in the production of biosurfactants. Biosurfactants have gained more attention in biotechnology industries as they are renewable and generally have superior properties to chemically synthesized compounds (Stainsby et al. 2022). They can be produced from various substrates and also be applied to environmental bioremediation (Mnif and Ghribi 2015; Stainsby et al. 2022). The production of biofuels was another application verified among the studies involving actinomycetes. El-Sheekh et al. (2017) evaluated the ability of actinomycetes to produce fatty acids and lipids, with potential use as biodiesel compared to that from microalgae. The results indicated that the best lipid producer was the species Streptomyces coelicolor, and the gross heating value of bacterial biodiesel (43,426 kJ kg⁻¹) was higher than that of algae biodiesel (41,896 kJ kg⁻¹). Buraimoh et al. (2021) used sugarcane bagasse residues as a renewable raw material to produce bioethanol using Streptomyces coelicolor. In the study, the strain was able to produce a significant amount of ethanol under aerobic conditions. Thus, the use of lignocellulose is a way of using residue from agricultural practices as a raw material, making the process cheaper and producing value-added biomolecules. Actinomycetes are of industrial interest since they are capable of decomposing plant biomass under different conditions, including high temperatures, varied pH values, toxic or aerobic environments, in addition to being able to produce enzymes, in this way, actinomycetes can be used in the sustainable production of biofuels (Balagurunathan et al. 2020).

Approximately 90% of known actinomycetes genera have been isolated from soil, these have been applied in several sectors (Sapkota et al. 2020). It is known that most new antibiotics were found by screening soil isolates (Sapkota et al. 2020). However, due to the emergence of multidrug-resistant pathogens, antimicrobial resistance is increasing, which is a problem for public health (Sapkota et al. 2020; Sarika et al. 2021). In this sense, more research is needed in this area to discover new antibiotics that help control the spread of diseases. Furthermore, it is important to search for new groups of actinomycetes from unexplored habitats, as they may be sources of new secondary metabolites (Davies-Bolorunduro et al. 2021). The use of actinomycetes in bioremediation processes is also a highlighted application. These microorganisms can be found in contaminated sites due to their resistance to polluting conditions. Thus, many actinomycetes present great potential for bioremediation uses as they are capable to treat several organic and inorganic contaminants (Farda et al. 2022; Sarkar Suthindhiran 2022; Timková et al. 2018). These microorganisms have applicability in the bioremediation of emerging contaminants (Kamaraj et al. 2022), polycyclic aromatic hydrocarbons (Hu et al. 2020), phenols (Barik et al. 2021), heavy metals (Baltazar et al. 2019), and dyes (Sundarajoo et al. 2022).

Based on all the presented applications, actinomycetes can contribute to achieve several Sustainable Development Goals (SDGs) of the United Nations, especially those related to food security and sustainable agriculture (SDG 2—Zero Hunger), human health (SDG 3—Good Health and Well-Being), water and soil treatment, biodiversity maintenance and soil fertility (SDG 6—Clean Water and Sanitation; SDG 14—Life Below Water; SDG 15—Life on Land), and biofuels production (SDG 7—Affordable and Clean Energy; SDG 13—Climate Action). Figure 3 summarizes the different functionalities of soil actinomycetes for pharmaceutical, food, agricultural, and environmental applications.

Fig. 3.

Potential uses of soil actinomycetes for pharmaceutical, food, agricultural, and environmental applications

Conclusions and perspectives

This review presented the main focus of the works about actinomycetes isolated from soil, which were the isolation and screening of new strains and the evaluation of their potential for pharmaceutical, food, agricultural and environmental uses. Regarding the main applications of actinomycetes, studies have focused on antimicrobial potential, enzymes production, agricultural uses, bioremediation, cosmetology, biofuels, and others related to their secondary metabolites production.

Actinomycetes can grow in different and unfavorable conditions, even in extreme environments, such as deserts, Antarctica, and deep marine soils and sediments. According to the reviewed articles, the main isolation locals of actinomycetes were Asia (especially China), Middle East, Sahara Desert, and Antarctica. Furthermore, these microorganisms are capable of growing in a wide range of temperature (4–60 °C; optimum: 28 °C), pH: (3–13; optimum: 7), and NaCl toleration (up to 32%; optimum: 0–1%). Streptomyces was the genus with the highest incidence among the actinomycetes isolated from soil and the most exploited for different uses. Because of the abundance and high tolerance to several substances and environments, actinomycetes are promising microorganisms for different industrial interests.

Author contributions

Conceptualization: Mateus Torres Nazari; Methodology: Mateus Torres Nazari; Formal analysis and investigation: Mateus Torres Nazari, Bruna Strieder Machado, Giovana Marchezi, Larissa Crestani, Valdecir Ferrari; Writing—original draft preparation: Mateus Torres Nazari, Bruna Strieder Machado, Giovana Marchezi, Larissa Crestani; Writing—review and editing: Mateus Torres Nazari, Valdecir Ferrari; Luciane Maria Colla, Jeferson Steffanello Piccin; Supervision: Luciane Maria Colla, Jeferson Steffanello Piccin.

Funding

This study was financed in part by the National Council for Scientific and Technological (CNPq) (Projects Codes 403658/2020–9 and 140541/2021–7) and the Coordination for the Improvement of Higher Education Personnel (CAPES).

Declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.