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Frontiers in Microbiology logoLink to Frontiers in Microbiology
. 2017 May 1;8:760. doi: 10.3389/fmicb.2017.00760

Deep Sea Actinomycetes and Their Secondary Metabolites

Manita Kamjam 1, Periyasamy Sivalingam 1, Zinxin Deng 1, Kui Hong 1,*
PMCID: PMC5410581  PMID: 28507537

Abstract

Deep sea is a unique and extreme environment. It is a hot spot for hunting marine actinomycetes resources and secondary metabolites. The novel deep sea actinomycete species reported from 2006 to 2016 including 21 species under 13 genera with the maximum number from Microbacterium, followed by Dermacoccus, Streptomyces and Verrucosispora, and one novel species for the other 9 genera. Eight genera of actinomycetes were reported to produce secondary metabolites, among which Streptomyces is the richest producer. Most of the compounds produced by the deep sea actinomycetes presented antimicrobial and anti-cancer cell activities. Gene clusters related to biosynthesis of desotamide, heronamide, and lobophorin have been identified from the deep sea derived Streptomyces.

Keywords: deep sea, actinomycetes, bioactive natural products, biosynthesis, novel species

Introduction

The search and discovery of novel microbes that produce new secondary metabolites can be expected to remain significant in the race against new and emerging diseases and antibiotic resistant pathogens (Berdy, 2012; Manivasagan et al., 2013). Actinomycetes are widely distributed in various marine habitats, ranging from sea sand (Hong et al., 2008), mangrove sediments (Hong et al., 2009; Hong, 2013; Azman et al., 2015), sea water (Zhang L. et al., 2012), coastal sediments (Yu et al., 2015), and deep sea sediments (Zhang et al., 2015; Chen et al., 2016). The increasing number of literature on marine actinomycetes strongly supported the view that marine environments including deep sea are significant sources for search and discovery of both diverse actinomycetes resources and secondary metabolites (Skropeta and Wei, 2014; Xu et al., 2014).

Deep sea habitats show extreme variations in available nutrients, light, oxygen concentration, pressure, salinity, and temperature. Deep-sea organisms have developed unique biochemical metabolic and physiological capabilities, which not only ensure their survival in this habitat but also provide potential for the production of novel metabolites absent in terrestrial microorganisms (Fenical, 1993; Bull et al., 2000; Skropeta and Wei, 2014). Through molecular ecology studies, actinobacterial operational taxonomic units (OTUs) have been identified from deep sea sediments. Most of those foreseeably exhibit novel species, genera and families (Stach and Bull, 2005; Chen et al., 2016). Diverse species of actinomycetes cultured from the deep seafloor surface, including the deepest sea sediment samples from the Mariana Trench, have shown great biosynthetic capacities and thus a potent source of novel natural products (Pathom-aree et al., 2006d; Abdel-Mageed et al., 2010). With the breakthrough of technological barriers associated with deep sea actinobacteria isolation strategies, such as sample collection and cultivation under standard laboratory conditions, more and more deep sea actinobacteria and their natural products have been identified. Here we review the recent progress on deep sea actinomycetes and their metabolites from literature during year 2006–2016.

Deep sea environment and biodiversity

The vast oceans cover 70% of the world's surface, with 95% greater than 1,000 m deep. Deep sea environments are divided into the bathyal zone (depths between 200 and 2,000 m), the abyssal (depths between 2,000 and 6,000 m) and the hadal zone (depths below 6,000 m) (Harino et al., 2009). Below sea level pressure is increased by depth, thereby in the deepest part of the trenches, the pressure varying from 10 atm at the shelf- slope interface to >1,000 atm. At bathyal depths temperatures taper off rapidly with increasing depth to 2°C. Deep-sea species must adjust their biochemical processes to survive in low temperatures, because the cold reduces chemical reaction rates. Oxygen concentration drops along with the depth, oxygen-minimum layer in mid-water, usually between 300 and 1,000 m depth. Light intensity decreases exponentially with depth in the water column. No photosynthetically useful light reaches the sea floor below about 250 m (Thistle, 2003).

Start at about 200 m depth, the deep sea is characterized by high pressure, low temperature, lack of light and variable salinity and oxygen concentration (Das et al., 2006), at the shelf break, where a clear change of fauna from shallow to deep water is observed (Thistle, 2003). According to Haefner (2003), in cold deep sea mud the diversity of life can be remarkably high with species richness rivaling that of tropical rain forest. Studying the species level of microbial diversity, finding a large number of rare species which more than half of them considered as new species and more than 95% is unidentified, furthermore the expanding of biodiversity reach to the 5,000 m in depth to abyssal which the peak amount of species at the depths of 3,000 m and beyond (Skropeta, 2008). On earth abyssal hills are the most abundant of biomass, but on wider abyss the ecological impact of the habitat heterogeneity is largely unexplored (Durden et al., 2015).

Deep sea actinomycetes cultivation

However, so far only a few actinomycetes have been isolated from deep sea. It is because of technological barriers associated with isolation strategies. Therefore, we are in the pace to develop efficient cultivation methods to recover the actinobacteria population from extreme deep sea habitats. To achieve the task, firstly collection of samples from deep sea plays a pivotal role. In recent years several advancements have been developed in the context of sample collection from deep sea such as modified sediment grab and designer-built bounce corer (Fenical and Jensen, 2006), remote-operated submarine vehicle (Pathom-aree et al., 2006d), neuston sampling devices (Hakvåg et al., 2008), multi-core sampler (Xu et al., 2009), gravity or piston cores (D'Hondt et al., 2009), and untethered coring device (Prieto-Davó et al., 2013).

It is crucial to cultivate deep sea actinomyetes under standard laboratory conditions. There are several factors that influence the isolation, such as pre-treatment of dry heat (Shin et al., 2008), media composition (Luo et al., 2011; Pan et al., 2013; Song et al., 2015), dilution factor (Pathom-aree et al., 2006a), seawater requirement (Song et al., 2015), artificial seawater (Pan et al., 2013; Pesic et al., 2013) and incubation time (Song et al., 2015). It has also shown the addition of different antibiotics on selective media can inhibit the growth of fungal and bacterial contamination in order to enhance the actinomycetes growth similar to those used in isolation of actinomycetes from terrestrial sample. Long term freeze storage of deep sea sediment samples at −80°C has shown to prevent the growth of fast-growing bacteria which in results enhance the actinomycetes population (Ulanova and Goo, 2015). For the initial isolation of Streptomyces, cultivation temperatures have also influenced the recovery from deep sea sediment samples. Optimal growth temperature generally ranging from 25 to 30°C for successful cultivation of deep sea actinomycetes (Jeong et al., 2006; Luo et al., 2011; Pesic et al., 2013).

Heat pre-treatment procedures have been used effectively for the selective isolation of members of several actinomycete taxa and also inhibited growth of bacterial and fungal colonies. Moreover, actinomycete spores and hyphae are more sensitive to wet than dry heat hence relatively low temperature regimes are used to pretreat water and soil suspensions. Although heat pretreatment procedures decrease the ratio of bacteria to actinomycetes on isolation plates, the numbers of actinomycetes may also be reduced (Williams et al., 1972; Pathom-aree et al., 2006a,b,c,d). Pathom-aree et al., isolated actinomycetes from Norwegian fjord sediments support that the numbers of actinomycetes were reduced when used heat pretreatment for isolation; fewer actinomycetes were isolated on selective media inoculated with suspensions treated at 55°C as opposed to 50°C. Similarly, higher counts were generally recorded on isolation plates seeded with non-heat pretreated suspensions (Pathom-aree et al., 2006d).

For the other method, Jensen et al., 2005 used dry and stamp method for isolation actinomycetes from tropical Pacific Ocean and found that using this method for isolation of actinomycetes showed good recovery of 44%. In addition, Ulanova and Goo (2015) found that the majority of actinomycete-like colonies were also isolated using dry stamping technique from subseafloor sediments at the Nankai and Okinawa Troughs.

Novel actinomycete species

Novel actinomycete species isolated from deep sea environment between 2006 and 2016, have yielded an impressive array of novel species with the highest number found at depths of abyssal zone and deeper. Different media has been used by researchers (Table 1). It is worth to be noticed that long time culturing and low temperature were employed for some of the novel isolates (Table 1). Only one novel Microbacterium marinum was obtained by pretreatment at 55°C, 6 min, others were from none heat pretreated samples (Table 1). The novel deep sea actinomycete species including 21 species under 13 genera with the maximum number from Microbacterium (n = 4), followed by Dermacoccus (n = 3), Streptomyces (n = 3) and Verrucosispora (n = 2), and one novel species for each of the other 9 genera (Table 1).

Table 1.

New actinomycetes species (n = 21) isolated from deep sea environment between 2006 and 2015.

Species Region Depth(m) Culture technique References
Extraction of act obact ria propagules/pretreatment procedure Media Incubation temperature and time
Amycolatopsis marina sp. nov. South China Sea Not sp cified Not specified SM1 with cycloheximide, neomycin sulfate and nystatin 28°C for 4 weeks Bian et al., 2009
Brevibacterium oceani sp. nov. Chagos Trench, Indian Ocean 5,904 Vortex sediment suspension in 2% NaCl for 1 min Yeast extract/peptone (YP) agar 15°C for 15 days Bhadra et al., 2008
Dermacoccus abyssi sp. nov. Mariana Trench (Challenger Deep) 10, 898 Shaking sediment suspension for 30 min at 150 rpm Raffinose-histidine agar with cycloheximide and nystatin 28°C for 12 weeks Pathom-aree et al., 2006a
Dermacoccus barathri sp. nov. Mariana Trench (Challenger Deep) 10, 898 Shaking sediment suspension for 30 min at 150 rpm Raffinose-histidine agar with cycloheximide and nystatin 28°C for 12 weeks Pathom-aree et al., 2006b
Dermacoccus profundi sp. nov. Mariana Trench (Challenger Deep) 10, 898 Shaking sediment suspension for 30 min at 150 rpm Raffinose-histidine agar with cycloheximide and nystatin 28°C for 12 weeks Pathom-aree et al., 2006b
Microbacterium indicum sp. nov. Chagos Trench, Indian Ocean 5,904 Vortex sediment suspension in 2% NaCl for 1 min Yeast extract/peptone (YP) agar 15°C for 15 days Shivaji et al., 2007
Microbacterium marinum sp. nov. South-west Indian Ocean 2,800 Heated sediment suspension in a water bath at 55°C for 6 min Modified DNB- seawater medium with nalidixic acid and nystatin 28°C for 1 week Zhang L. et al., 2012
Microbacterium profundi sp. nov. East Pacific polymetallic nodule region 5,280 Vortex sediment suspension in sterile seawater for 15 min Modified ZoBell medium 25°C for 2 weeks Wu et al., 2008
Microbacterium sediminis sp. nov. South-west Indian Ocean 2,327 Vortex sediment suspension in sterile seawater FJ sea water (50%) agar with rifampicin and potassiumdichromate 28°C Yu et al., 2013
Modestobacter marinus sp. nov. Atlantic Ocean 2,983 Not specified Not specified Not specified Xiao et al., 2011b
Myceligenerans cantabricum sp. nov. Avile's Canyon in the Ca tabrian Sea, Asturias, Spain 1,500 Not specified 1/3 tryptic soy agar and 1/6 M-BLEB sea water agar with cycloheximide and nystatin 28°C for 2 weeks Vizcaíno et al., 2015
Nesterenkonia alkaliphila sp. nov. Western Pacific Ocean 7,118 Not specified Modified ISP 1- seawater 28°C for 3 weeks Zhang et al., 2015
Pseudonocardia antitumoralis sp. nov. South China Sea 3,258 Not specified ISP 5- seawater medium 28°C for 3 weeks Tian et al., 2013
Sciscionella marina gen. nov., sp. nov. Northern South China Sea 516 Not specified Gauze No. 1 -seawater medium 28°C for 3 weeks Tian et al., 2009
Serinicoccus profundi sp. nov. Indian Ocean 5,368 Not specified Oligotrophic- seawater medium Not specified Xiao et al., 2011a
Streptomyces indicus sp. nov. Indian Ocean 2,434 Not specified Modified HV—sea water (75%) medium 25°C Luo et al., 2011
Streptomyces nanhaiensis sp. nov. South China Sea 1,632 Not specified Humic acid-vitamin- sea water (70%) medium 28°C for 3 weeks Tian et al., 2012a
Streptomyces oceani sp. nov. Northern South China Sea 578 Not specified 10 % Nutrient seawater agar 28°C for 3 weeks Tian et al., 2012b
Verrucosispora maris sp. nov. Sea of Japan Not specified Not specified Colloidal chitin agar 30°C for 4 weeks Goodfellow et al., 2012
Verrucosispora sediminis sp. nov. South China Sea 3,602 Not specified Gauze No. 1 medium 22°C for 4 weeks Dai et al., 2010
Williamsia marianensis sp. nov. Mariana Trench (Challenger Deep) 10, 898 Shaking sediment suspension for 30 min at 150 rpm Raffinose-histidine agar with cycloheximide and nystatin 28°C for 12 weeks Pathom-aree et al., 2006c

SM1*: yeast nitrogen base (67.0 g; Difco) and casamino acids (100 mg; Difco) are added to a liter of distilled water and the solution sterilized using cellulose filters (0.20 mm) prior to the addition of sterilized dipotassium hydrogen phosphate (200 ml; 10%,w/v);100 ml of this basal medium was added to 900 ml of sterilized molten agar (1.5%,w/v) followed by filter ster l sed solutions of D (−) sorbitol (final concentration 1%,w/v); YP agar* per liter distilled water: 5 g, yeast extract, 10 g peptone, 30 g NaCl, 15 g agar; Raffinose-h st d ne agar*: Raffinose 10 g, L-histidine 1 g, MgSO4 7H2O 0.5 g, FeSO4 7H2O 0.01g, K2HPO4 1 g, Agar 20 g, pH 7.0-7.4; Modified DNB medium*: 0.1 g p ptone, 0.05 g b f xtract, 0.05 g NaCl, 1000 mL artificial seawater, pH 7.5; Modified ZoBell agar*: 19.45 g NaCl, 8.8 g MgCl2, 3.24 g Na2SO4, 1.8 g CaCl 2, 0.55 g KCl, 0.16 g NaHCO3, 0.1 g f rric citrate pentahydrate, 80 mg KBr, 34 mg CsCl2, 22 mg H3BO3, 4.0 mg Na2SiO3, 2.4 mg NaF, 1.6 mg, NH4NO3, 8.0 mg Na 3PO4, 0.5 g p pton, 0.1 g yeast extract, 20 g agar (pH 5.5, adjusted with HCl); FJ agar*: 1% glucose, 1% yeast extract, 1.5% agar, 50% seawater; 1/3 tryptic soy agar and 1/6 M-BLEB*: 1/3 tryptic soy agar (TSA, Merck) and 1/6 M-BLEB [9 g MOPS BLEB base (Oxoid) in 1 l Cantabrian Sea water], agar; Modified SP 1*: (1 L atural seawate, pH 10 final): 10 g glucose, 5 g peptone, 5 g yeast extract, 0.2 g MgSO4. 7H2O, 10 g NaHCO3, 27 g Na2 CO3 10H2O and 15 g agar; ISP 5 medium*: L-asparagine (anhydrous basis) 1.0 g, Glycerol 10.0 g, K2HP04 (anhydrous basis) 1.0 g, natural seawater 1. 0 l, Trace salts solution 1.0 ml Agar 20.0 g; SM3*: glucose 10 g, peptone 5 g, tryptone 3 g, NaCl 5 g, agar 15 g, distilled water, 1 l, pH 7.0; Gauze No. 1 medium*: Soluble starch 20.0 g, KNO3 1.0 g, NaCl 0.5 g, MgSO4 x 7 H2O 0.5 g, K2HPO4 0.5 g, FeSO4 x 7 H2O 10.0 mg, Agar 15.0 g, Sea water 1.0 L, Adjust pH 7.4; Oligotrophic- seawater medium*: Oligotrophic medium (seawater, 2.0% agar); Modified HV medium*: humic acid 1.0 g, KCl 1.7 g, FeSO4. 7H2O 0.01 g, Na2HPO4 0.5 g, MgSO4. 7H2O 0.5 g, CaCO3 0.02 g, thiamine 0.5 mg, nicotinic acid 0.5 mg, pantothenic acid 0.5 mg, p-aminobenzoic acid 0.5 mg, riboflavin 0.5 mg, vitamin B6 0.5 mg, inositol 0.5 mg, biotin 0.25 mg, water 250 ml, seawater 750 ml, agar 18 g, pH 7.2; Humic acid-vitamin agar*: Humic acid 2g, Asparagine 1 g, K2HPO4 0.5 g, FeSO4 7H2O 0.5 g, Agar 20 g, Sea-water 1000 ml, pH 7.0–7.4; 10% Nutrient agar*: Beef extract 0.03 g, peptone 0.05 g, agar 15 g, sea water 1 L; colloidal chitin agar*: 4 g of chitin, K2HPO4 (0.7 g); KH2PO, (0.3 g); MgSO4-5H2O (0.5 g); FeSO4.7H20 (0.01 g); ZnSO4 (0.001 g); MnCl1, (0.001 g); and 20 g of agar. pH 8.0

Natural products synthesized by deep sea actinomycetes

The numbers of novel microbial metabolites from deep sea sediment samples have been increasing, especially from deep sea streptomycetes. Eight genera of actinomycetes were reported to produce secondary metabolites, among which Streptomyces is the richest producer (Table 2). Earlier culture dependent studies strongly suggested that Streptomyces species are present in considerable number in deep sea sediment samples (Jensen et al., 2005; Pathom-aree et al., 2006d). In addition several novel species of deep sea derived Streptomyces strains with distinct metabolites have been reported which indicates deep sea Streptomyces are really worth in the context of novel natural products discovery (Pan et al., 2015; Song et al., 2015).

Table 2.

Natural products synthesized by deep sea actinomycetes.

Strain Compounds Region Depth (m) Bioactivity References
Dermacoccus abyssi Dermacozines A–G Mariana Trench (Challenger Deep) 10, 898 Moderate cytotoxic activity against the leukemia cell line K562 Abdel-Mageed et al., 2010
Dermacoccus abyssi Dermacozines H-J Mariana Trench (Challenger Deep) 10, 898 Radical scavenging activity Wagner et al., 2014
Marinactinospora thermotolerans Marinacarbolines A–D, Indolactam alkaloids South China Sea 3,865 Strong antiplasmodial activity Huang et al., 2011
Microbacterium sediminis sp.nov. Microbacterins A and B South-west Indian Ocean 2,327 Significatnt inhibitory effects against a panel of human tumor cell Liu D. et al., 2015
Micromonospora sp. Levantilides A and B Mediterranean 4,400 Anticancer Gärtner et al., 2011
Nocardiopsis alba SCSIO 03039 Methoxyneihumicin Indian Ocean Not specified Anticancer Zhang et al., 2013
Nocardiopsis sp. Nocardiopsins A and B Coast of Brisbane, Australia 55 No activity Raju et al., 2010
Pseudonocardia sp. Pseudonocardians A–C South China Sea 3,258 Anticancer, antibacterial activity Li et al., 2011
Serinicoccus profundi sp. nov. Indole alkaloid Indian Ocean 5,368 Antibacterial activity Yang et al., 2013b
Streptomyces cavourensis NA4 Bafilomycins B1 and C1 South China Sea 1,464 Antifungal Substances Pan et al., 2015
Streptomyces drozdowiczii SCSIO 10141 Marformycins South China Sea 1,396 Anti- infective Zhou et al., 2014
Streptomyces fungicidicus Diketopiperazines Western Pacific 5,000 Antifouling products Li et al., 2006
Streptomyces lusitanus Grincamycins B–F South China Sea 3,370 Anticancer Huang et al., 2012
Streptomyces niveus SCSIO 3406 Marfuraquinocins South China Sea 3,536 Cytotoxic, antibacterial activity Song et al., 2013
Streptomyces olivaceus FXJ8.012 Tetroazolemycins A and B Southwest Indian Ocean Not specified Metal ion-binding activity Liu et al., 2013
Streptomyces scopuliridis SCSIO ZJ46 D sotamides B−D South China Sea 3,536 Antibacterial activity Song et al., 2014
Streptomyces sp. Ammosamides A and B Bahamas 1,618 Anticancer Gaudêncio et al., 2008
Streptomyces sp. Benzoxacystol Atlantic 3,814 Inhibitory activity against the enzyme glycogen synthase kinase-3b Nachtigall et al., 2011
Streptomyces sp. Caboxamycin Atlantic 3,814 Inhibitory activity against Gram-positive bacteria, anticancer Hohmann et al., 2009
Streptomyces sp. Spiroindimicins A–D Indian Ocean 3,412 Anticancer Zhang W. J. et al., 2012
Streptomyces sp. Streptokordin Ayu Trough Not specified Anticancer Jeong et al., 2006
Streptomyces sp. Streptopyrrolidine Ayu Trough Not specified Anti-angiogenesis activity Shin et al., 2008
Streptomyces sp. ACT232 Ahpatinin Sagami Bay 1, 174 Aspartic protease inhibitors Sun et al., 2014
Streptomyces sp. SCSIO 01127 Lobophorins E and F South China Sea 1, 350 Antibacterial activity, cytotoxicity Niu et al., 2011
Streptomyces sp. SCSIO 03032 Heronamides D−F Indian Ocean 3,412 No activity Zhang W. et al., 2014
Streptomyces sp. SCSIO 03032 Indimicins Indian Ocean 3,412 Cytotoxic Zhang W. J. et al., 2014
Streptomyces sp. SCSIO 04496 (6R,3Z)-3-benzylidene-6-isobutyl-1-methyl piperazine-2,5-dione South China Sea 3,536 No activity Luo et al., 2015
Streptomyces sp. SCSIO 10355 Strepsesquitriol Indian Ocean 3,412 Inhibitory activity against lipopolysaccharide-induced TNFα production Yang et al., 2013a
Streptomyces sp. SCSIO 11594 Dehydroxyaquayamycin South China Sea 2,403 Antibacterial activity Song et al., 2015
Streptomyces sp. SCSIO 11594 Marangucycline B South China Sea 2,403 Anticancer Song et al., 2015
Streptomyces sp. SNJ013 Sungsanpin Jeju Island 138 Inhibitory activity to A549 with cell invasion assay Um et al., 2013
Streptomyces sp. UST040711-290 12-methyltetradecanoid acid (12-MTA) Pacific 5,774 Antifouling Xu et al., 2009
Streptomyces sp. TP-A0873 Butenolids Toyama Bay Not specified Peroxisome proliferator activated receptor—PPARα agonistic Igarashi et al., 2015; Komaki et al., 2015
Streptomyces sp. 12A35 Lobophorins H and I South China Sea 2,134 Antibacterial activity Pan et al., 2013
Streptomyces strain C42 Champacyclin Baltic Sea 241 Antimicrobial activity Pesic et al., 2013
Streptomyces xiamenensis M1-94P Xiamenmycin C and D Pacific Ocean 2,628 Anti-fibrotic You et al., 2013
Verrucosispora sp. Abyssomicins J–L South China Sea 2,733 Antibacterial activity Wang et al., 2013

The deepest sea sediment samples from the Mariana Trench have been shown to possess great biosynthetic capacities. Seven dermacozines A–G were reported from the actinobacteria Dermacoccus abyssi sp. nov., strains MT1.1 and MT1.2 isolated from Mariana Trench sediment collected at a depth of 10 898 m. Dermacozines F and G displayed moderate cytotoxic activity against the leukemia cell line K562 with IC50 values of 9 and 7 mM, respectively, whereas dermacozine C also exhibited high radical scavenger activity with an IC50 value of 8.4 mM (Abdel-Mageed et al., 2010).

In recent years, South China Sea has been emerging as a potentially abundant source of novel species/genera of marine actinomycetes. Some bioactive compounds, such as pseudonocardians A-C, grincamycins B-F, and abyssomicins J-L were reported. Natural products derived from deep sea actinomycetes discovery have displayed a wide range of bioactivities, such as antitumor, antimicrobial, antifouling, and anti-fibrotic activities (Table 2).

Biosynthesis pathways for deep sea streptomycetes natural products

Lobophorins H and I together with three known analogs, O-β-kijanosyl-(1 → 17)-kijanolide, lobophorins B and F were yielded by Streptomyces sp. 12A35, isolated from a deep sea sediment sample collected at a depth of 2,134 m in South China Sea (Pan et al., 2013). While, lobophorins E and F, along with two known analogs lobophorins A and B were discovered from the products of the deep sea Streptomyces sp. SCSIO 01127, was isolated from sample collected at a depth of 1,350 m in the South China Sea (Niu et al., 2011). The gene cluster involved in biosynthesis of lobophorin was the first type I PKS gene cluster identified from the deep sea derived Streptomyces. Three glycosyltransferases (GTs) LobG1-LobG3 genes-inactivation mutants yielded five different glycosylated metabolites, and the result suggested that LobG3 as an iterative GT to attach two L-digitoxoses (Li et al., 2013). Desotamides B, C and D together with a known desotamide A were obtained from deep sea derived Streptomyces scopuliridis SCSIO ZJ46, recovered from sediment sample collected at a depth of 3,536 m in the South China Sea (Song et al., 2014). A 39 kb gene cluster governing the biosynthesis of the anti-infective desotamides has been isolated from the strain. Desotamides A and B and a new desotamide G have been obtained by heterologous expression of desotamide gene cluster in Streptomyces coelicolor M1152 (Li et al., 2015).

Heronamides D, E, and Fare discovered from the products of Streptomyces sp. SCSIO 03032, which was isolated from deep sea sediment sample collected at a depth of 3,412 m in the Bay of Bengal, Indian Ocean (Zhang W. et al., 2014). The gene cluster governing the biosynthesis of heronamide has been isolated from strain SCSIO 03032. The gene inactivation study confirmed that P450 enzyme encode HerO as an 8-hydroxylase for tailoring heronamide biosynthesis. Feeding experiments with labeled small carboxylic acid molecules confirmed the migrated double bonds in the conjugated diene-containing side chain of heronamides (Zhu et al., 2015).

Marformycins A-F were obtained from fermentation broth of deep sea sediment-derived Streptomyces drozdowiczii SCSIO 1014, which was isolated from sample collected at a depth of 1,396 m in South China Sea. All compounds exerted selective anti-microbial activity against Micrococcus luteus, Propionibacterium acnes, and P. granulosum. Marformycins A-E displayed inhibitory activity against M. luteus with MICs of 0.25, 4.0, 0.25, 0.063, and 4.0 μg/mL, respectively, while they did not displayed any cytotoxicity (Liu D. et al., 2015). It is suggested that these compounds may be used as promising candidatures for anti-infective drug leads. The gene cluster that responsible for the biosynthesis of marformycin is about 45 kb in size and has been identified from strain SCSIO 10141. The gene inactivation studies indicated that three NRPS proteins MfnC, MfnD, MfnE, a free adenylation (A) enzyme MfnK, and a free peptidyl carrier protein (PCP) MfnL were essential for the generation of the marformycin core scaffold. Further, MfnN was found to use an intact cyclodepsipeptide intermediate as its substrate (Liu J. et al., 2015).

Perspective

The discovery of novel actinomycete taxa with unique metabolic activity from deep sea samples, and novel compounds with the greatest biogenic, metabolic diversity and biological activities clearly illustrate that indigenous deep sea actinomycetes indeed exist in the oceans and are an important source of novel secondary metabolites. Other function of deep sea actinobacteria is also interesting such as oil degradation and biosurfactant production (Wang et al., 2014). It is worth to be noticed that no heat pretreatment, dry and stamp method and low temperature incubation were more productive for actinomycetes isolation from some deep sea samples. With the development of culture independent techniques, more productive strategy of strain isolation guided by the deep sea actinomycetes distribution or direct cloning and heterologous express the functional genes could be approached.

Author contributions

MK contribute the introduction, deep sea environment and biodiversity, actinomycete cultivation, novel taxa, and Table 1. PS contribute sample collection, Table 2 and biosynthesis of secondary metabolites from deep sea streptomycetes. KH and ZD conceived the idea and revised the whole manuscript.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The work described here was partially supported by the EU FP7 project PharmaSea (312184).

References

  1. Abdel-Mageed W. M., Milne B. F., Wagner M., Schumacher M., Sandor P., Pathom-aree W., et al. (2010). Dermacozines, a new phenazine family from deep-sea dermacocci isolated from a Mariana Trench sediment. Org. Biomol. Chem. 8, 2352–2362. 10.1039/c001445a [DOI] [PubMed] [Google Scholar]
  2. Azman A. S., Othman I., Velu S. S., Cha K. G., Lee L. H. (2015). Mangrove rare actinobacteria: taxonomy, natural compound, and discovery of bioactivity. Front. Microbiol. 6:856. 10.3389/fmicb.2015.00856 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berdy J. (2012). Thoughts and facts about antibiotics: where we are now and where we are heading. J. Antibiot. 65, 385–395. 10.1038/ja.2012.27 [DOI] [PubMed] [Google Scholar]
  4. Bhadra B., Raghukumar C., Pindi P. K., Shivaji S. (2008). Brevibacterium oceani sp. nov., isolated from deep-sea sediment of the Chagos Trench, Indian ocean. Int. J. Syst. Evol. Microbiol. 58, 57–60. 10.1099/ijs.0.64869-0 [DOI] [PubMed] [Google Scholar]
  5. Bian J., Li Y., Wang J., Song F. H., Liu M., Dai H. Q., et al. (2009). Amycolatopsis marina sp. nov., an actinomycete isolated from an ocean sediment. Int. J. Syst. Evol. Microbiol. 59, 477–481. 10.1099/ijs.0.000026-0 [DOI] [PubMed] [Google Scholar]
  6. Bull A. T., Ward A. C., Goodfellow M. (2000). Search and discovery strategies for biotechnology: the paradigm shift. Microbiol. Mol. Biol. Rev. 64, 573–606. 10.1128/MMBR.64.3.573-606.2000 [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen P., Zhang L., Guo X., Dai X., Liu L., Xi L., et al. (2016). Diversity, biogeography, and biodegradation potential of actinobacteria in the deep-sea sediments along the deep sea sediments along the Southwest Indian Ridge. Front. Microbiol. 7:1340. 10.3389/fmicb.2016.01340 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. D'Hondt S., Spivack A., Pockalny R., Ferdelman T., Fischer J., Kallmeyer J., et al. (2009). Sub seafloor sedimentary life in the South Pacific Gyre. Proc. Natl. Acad. Sci. U.S.A. 106, 11651–11656. 10.1073/pnas.0811793106 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dai H. Q., Wang J., Xin Y. H., Pei G., Tang S. K., Ren B., et al. (2010). Verrucosispora sediminis sp. nov., a cyclodipeptide- producing actinomycete from deep-sea sediment. Int. J. Syst. Evol. Microbiol. 60, 1807–1812. 10.1099/ijs.0.017053-0 [DOI] [PubMed] [Google Scholar]
  10. Das S., Lyla P., Khan S. A. (2006). Marine microbial diversity and ecology: importance and future perspectives. Curr. Sci. 90, 1325–1335. [Google Scholar]
  11. Durden J. M., Bett B. J., Jones D. O. B., Huvenne V. A. I., Ruhl H. A. (2015). Abyssal hills hidden source of increased habitat heterogeneity, benthic megafaunal biomass and diversity in the deep sea. Prog. Oceanogr. 137, 209–218. 10.1016/j.pocean.2015.06.006 [DOI] [Google Scholar]
  12. Fenical W. (1993). Chemical studies of marine bacteria: developing a new resource. Chem. Rev. 93, 1673–1683. 10.1021/cr00021a001 [DOI] [Google Scholar]
  13. Fenical W., Jensen P. R. (2006). Developing a new resource for drug discovery: marine actinomycete bacteria. Nat. Chem. Biol. 2, 666–673. 10.1038/nchembio841 [DOI] [PubMed] [Google Scholar]
  14. Gärtner A., Ohlendorf B., Schulz D., Zinecker H., Wiese J., Imhoff J. F. (2011). Levantilides A and B, 20-membered Macrolides from a Micromonospora strain isolated from the Mediterranean deep sea sediment. Mar. Drugs 9, 98–108. 10.3390/md9010098 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gaudêncio S. P., MacMillan J. B., Jensen P. R., Fenical W. (2008). Ammosamides A and B new cytotoxic alkaloids isolated from a marine Streptomyces sp. Planta Med. 74:PB172 10.1055/s-0028-1084516 [DOI] [Google Scholar]
  16. Goodfellow M., Stach J. E., Brown R., Bonda A. N., Jones A. L., Mexson J., et al. (2012). Verrucosispora maris sp. nov., a novel deep-sea actinomycete isolated from a marine sediment which produces abyssomicins. Antonie van Leeuwenhoek 101, 185–193. 10.1007/s10482-011-9651-5 [DOI] [PubMed] [Google Scholar]
  17. Haefner B. (2003). Drugs from the deep: marine natural products as drug candidates. Drug Discov. Today 8, 536–544. 10.1016/S1359-6446(03)02713-2 [DOI] [PubMed] [Google Scholar]
  18. Hakvåg S., Fjaervik E., Josefsen K. D., Ian E., Ellingsen T. E., Zotchev S. B. (2008). Characterization of Streptomyces spp. isolated from the sea surface microlayer in the Trondheim Fjord, Norway. Mar. Drugs 6, 620–635. 10.3390/md6040620 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Harino H., Arai T., Ohji M., Miyazaki N. (2009). Organotin contamination in deep sea environment, in Ecotoxicology of Antifouling Biocides, eds Arai T., Harino H., Ohji M., Langston W. J. (New York, NY: Springer; ), 95–97. 10.1007/978-4-431-85709-9_6 [DOI] [Google Scholar]
  20. Hohmann C., Schneider K., Brunter C., Irran E., Nicholson G., Bull A. T., et al. (2009). Caboxamycin, a new antibiotic of the benzoxazole family produced by the deep-sea strain Streptomyces sp. NTK 937. J. Antibiot. 62, 99–104. 10.1038/ja.2008.24 [DOI] [PubMed] [Google Scholar]
  21. Hong K. (2013). Actinomycetes from mangrove and their secondary metabolites. Acta Microbiol. Sin. 53, 1131–1141 [PubMed] [Google Scholar]
  22. Hong K., Gao A. H., Xie Q. Y., Gao H., Zhuang L., Lin H. P., et al. (2009). Actinomycetes for marine drug discovery isolated from mangrove soils and plants in China. Mar. Drugs 7, 24–44. 10.3390/md7010024 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hong S. G., Lee Y. K., Yim J. H., Chun J., Lee H. K. (2008). Sanguibacter antarcticus sp. nov., isolated from Antarctic sea sand. Int. J. Syst. Evol. Microbiol. 58, 50–52. 10.1099/ijs.0.65031-0 [DOI] [PubMed] [Google Scholar]
  24. Huang H. B., Yang T. T., Ren X. M., Liu J., Song Y. X., Sun A. J., et al. (2012). Cytotoxic Angucycline class glycosides from the deep sea actinomycete Streptomyces lusitanus SCSIO LR32. J. Nat. Prod. 75, 202–208. 10.1021/np2008335 [DOI] [PubMed] [Google Scholar]
  25. Huang H. B., Yao Y. L., He Z. X., Yang T. T., Ma J. Y., Tian X. P., et al. (2011). Antimalarial β-carboline andindolactam alkaloids from Marinactinospora thermotolerans a deep sea isolate. J. Nat. Prod. 74, 2122–2127. 10.1021/np200399t [DOI] [PubMed] [Google Scholar]
  26. Igarashi Y., Ikeda M., Miyanaga S., Kasai H., Shizuri Y., Matsuura N. (2015). Two butenolides with PPARα agonistic activity from a marine-derived Streptomyces. J. Antibiot. 68, 345–347. 10.1038/ja.2014.151 [DOI] [PubMed] [Google Scholar]
  27. Jensen P. R., Mincer T. J., Williams P. G., Fenical W. (2005). Marine actinomycete diversity and natural product discovery. Antonie Van Leeuwenhoek 87, 43–48. 10.1007/s10482-004-6540-1 [DOI] [PubMed] [Google Scholar]
  28. Jeong S. Y., Shin H. J., Kim T. S., Lee H. S., Park S. K., Kim H. M. (2006). Streptokordin, a new cytotoxic compound of the methylpyridine class from a marine-derived Streptomyces sp. KORDI-3238. J. Antibiot. 59, 234–240. 10.1038/ja.2006.33 [DOI] [PubMed] [Google Scholar]
  29. Komaki H., Ichikawa N., Hosoyama A., Fujita N., Igarashi Y. (2015). Draft genome sequence of marine-derived Streptomyces sp. TP-A0873, a producer of a Pyrrolizidine alkaloid bohemamine. Genome Announc. 3, e00008–e00015. 10.1128/genomea.00008-15 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Li Q., Song Y., Qin X., Zhang X., Sun A., Ju J. (2015). Identification of the biosynthetic gene cluster for the anti-infective desotamides and production of a new analogue in a heterologous host. J. Nat. Prod. 78, 944–948. 10.1021/acs.jnatprod.5b00009 [DOI] [PubMed] [Google Scholar]
  31. Li S., Tian X., Niu S., Zhang W., Chen Y., Zhang H., et al. (2011). Pseudonocardians AC, new Diazaanthraquinone derivatives from a deap sea actinomycete Pseudonocardia sp. SCSIO 01299. Mar. Drugs 9, 1428–1439. 10.3390/md9081428 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Li S., Xiao J., Zhu Y., Zhang G., Yang C., Zhang H., et al. (2013). Dissecting glycosylation steps in lobophorin biosynthesis implies an iterative glycosyltransferase. Org Lett. 15, 1374–1377. 10.1021/ol400342e [DOI] [PubMed] [Google Scholar]
  33. Li X., Dobretsov S., Xu Y., Xiao X., Hung O. X., Qian P. Y. (2006). Antifouling diketopiperazines produced by a deep-sea bacterium, Streptomyces fungicidicus. Biofouling 22, 201–208. 10.1080/08927010600780771 [DOI] [PubMed] [Google Scholar]
  34. Liu D., Lin H., Proksch P., Tang X., Shao Z., Lin W. (2015). Microbacterins A and B, new peptaibols from the deep sea actinomycete Microbacterium sediminis sp. nov. YLB-01(T). Org Lett. 17, 1220–1223. 10.1021/acs.orglett.5b00172 [DOI] [PubMed] [Google Scholar]
  35. Liu J., Wang B., Li H., Xie Y., Li Q., Qin X., et al. (2015). Biosynthesis of the antiinfective marformycins featuring pre-NRPS assembly line N-formylation and Omethylation and post-assembly line C-hydroxylation chemistries. Org Lett. 17, 1509–1512. 10.1021/acs.orglett.5b00389 [DOI] [PubMed] [Google Scholar]
  36. Liu N., Shang F., Xi L. J., Huang Y. (2013). Tetroazolemycins A and B, two new oxazole-thiazole siderophores from deep-sea Streptomyces olivaceus FXJ8.012. Mar. Drugs 11, 1524–1533. 10.3390/md11051524 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Luo M. H., Tang G. L., Jub J. H., Lua L. C., Huang H. B. (2015). A new diketopiperazine derivative from a deep sea-derived Streptomyces sp. SCSIO 04496. Nat. Prod. Res. 30, 1–6. 10.1080/14786419.2015.1045509 [DOI] [PubMed] [Google Scholar]
  38. Luo Y., Xiao J., Wang Y., Xu J., Xie S., Xu J. (2011). Streptomyces indicussp. nov., an actinomycete isolated from deep-sea sediment. Int. J. Syst. Evol. Microbiol. 61, 27126. 10.1099/ijs.0.029389-0 [DOI] [PubMed] [Google Scholar]
  39. Manivasagan P., Venkatesan J., Sivakumar K., Kim S. K. (2013). Marine actinobacterial metabolites: current status and future perspectives. Microbiol. Res. 168, 311–332. 10.1016/j.micres.2013.02.002 [DOI] [PubMed] [Google Scholar]
  40. Nachtigall J., Schneider K., Bruntner C., Bull A. T., Goodfellow M., Zinecker H. (2011). Benzoxacystol, a benzoxazine-type enzyme inhibitor from the deep-sea strain Streptomyces sp. NTK 935. J. Antibiot. 64, 453–457. 10.1038/ja.2011.26 [DOI] [PubMed] [Google Scholar]
  41. Niu S., Li S. M., Chen Y., Tian X. P., Zhang H. B., Zhang G. T., et al. (2011). Lobophorins E and F, new spirotetronate antibiotics from a South China sea-derived Streptomyces sp. SCSIO 01127. J. Antibiot. 64, 711–716. 10.1038/ja.2011.78 [DOI] [PubMed] [Google Scholar]
  42. Pan H. Q., Yu S. Y., Song C. F., Wang N., Hua H. M., Hu J. C., et al. (2015). Identification and characterization of the antifungal substances of a novel Streptomyces cavourensis NA4. J. Ind. Microbiol. Biotechnol. 25, 353–357. 10.4014/jmb.1407.07025 [DOI] [PubMed] [Google Scholar]
  43. Pan H. Q., Zhang S. Y., Wang N., Li Z. L., Hua H. M., Hu J. C., et al. (2013). New spirotetronate antibiotics lobophorins H and I from a South China sea derived Streptomyces sp. 12A35. Mar. Drugs 11, 3891–3901. 10.3390/md11103891 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pathom-aree W., Nogi Y., Sutcliffe L. C., Ward A. C., Horikoshi K., Bull A. T., et al. (2006a). Dermacoccus abyssi sp. nov., a piezotolerant actinomycete isolated from the Mariana Trench. Dermacoccus abyssi sp. nov., a piezotolerant actinomycete isolated from the Mariana Trench. Int. J. Syst. Evol. Microbiol. 56 1233–1237. 10.1099/ijs.0.64133-0 [DOI] [PubMed] [Google Scholar]
  45. Pathom-aree W., Nogi Y., Sutcliffe L. C., Ward A. C., Horikoshi K., Bull A. T., et al. (2006b). Dermacoccus barathri sp. nov. and Dermacoccus profundi sp. nov., novel actinomycetes isolated from deep-sea mud of the Mariana Trench. Int. J. Syst. Evol. Microbiol. 56, 2303–2307. 10.1099/ijs.0.64250-0 [DOI] [PubMed] [Google Scholar]
  46. Pathom-aree W., Nogi Y., Sutcliffe L. C., Ward A. C., Horikoshi K., Bull A. T., et al. (2006c). Williamsia marianensis sp. nov., a novel actinomycete isolated from the Mariana Trench. Int. J. Syst. Evol. Microbiol. 56, 1123–1126. 10.1099/ijs.0.64132-0 [DOI] [PubMed] [Google Scholar]
  47. Pathom-aree W., Stach J. E., Ward A. C., Horikoshi K., Bull A. T., Goodfellow M. (2006d). Diversity of actinomycetes isolated from Challenger deep sediment (10,898 m) from the Mariana Trench. Extremophiles 10, 181–189. 10.1007/s00792-005-0482-z [DOI] [PubMed] [Google Scholar]
  48. Pesic A., Baumann H. I., Kleinschmidt K., Ensle P., Wiese J., Süssmuth R. D., et al. (2013). Champacyclin, a new cyclic octapeptide from Streptomyces strain C42 isolated from the Baltic Sea. Mar Drugs 11, 4834–4857. 10.3390/md11124834 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Prieto-Davó A., Villarreal-Gómez L. J., Forschner-Dancause S., Bull A. T., Stach J. E., Smith C., et al. (2013). Targeted search for actinomycetes from nearshore and deep sea marine sediments. FEMS Microbiol Ecol. 84, 510–518. 10.1111/1574-6941.12082 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Raju R., Piggott A. M., Conte M., Tnimov Z., Alexandrov K., Capon R. J. (2010). Nocardiopsins: new FKBP12-binding macrolide polyketides from an Australian marinederived actinomycete, Nocardiopsis sp. Chem. Eur. J. 16, 3194–3200. 10.1002/chem.200902933 [DOI] [PubMed] [Google Scholar]
  51. Shin H. J., Kim T. S., Lee H. S., Park J. Y., Choi I. K., Kwon H. J. (2008). Streptopyrrolidine, an angiogenesis inhibitor from a marine-derived Streptomyces sp. KORDI-3973. Phytochemistry 69, 2363–2366. 10.1016/j.phytochem.2008.05.020 [DOI] [PubMed] [Google Scholar]
  52. Shivaji S., Bhadra B., Rao R. S., Chaturvedi P., Pindi P. K., Raghukumar C. (2007). Microbacterium indicum sp. nov., isolated from a deep-sea sediment sample from the Chagos Trench, Indian Ocean. Int. J. Syst. Evol. Microbiol. 57, 1819–1822. 10.1099/ijs.0.64782-0 [DOI] [PubMed] [Google Scholar]
  53. Skropeta D. (2008). Deep-sea natural products. Nat. Prod. Rep. 25, 1131–1166. 10.1039/b808743a [DOI] [PubMed] [Google Scholar]
  54. Skropeta D., Wei L. (2014). Recent advances in deep-sea natural products. Nat. Prod. Rep. 31, 999–1025. 10.1039/C3NP70118B [DOI] [PubMed] [Google Scholar]
  55. Song Y., Huang H. B., Chen Y. C., Ding J. C., Zhang Y., Sun A., et al. (2013). Cytotoxic and antibacterial Marfuraquinocins from the deep South China sea-derived Streptomyces niveus SCSIO 3406. J. Nat. Prod. 76, 2263–2268. 10.1021/np4006025 [DOI] [PubMed] [Google Scholar]
  56. Song Y., Li Q., Liu X., Chen Y., Zhang Y., Sun A., et al. (2014). Cyclic hexapeptides from the deep south China sea-derived Streptomyces scopuliridis SCSIO ZJ46 active against pathogenic gram-positive bacteria. J. Nat. Prod. 77, 1937–1941. 10.1021/np500399v [DOI] [PubMed] [Google Scholar]
  57. Song Y., Liu G., Li J., Huang H., Zhang X., Zhang H., et al. (2015). Cytotoxic and antibacterial Angucycline- and Prodigiosin- analogues from the deep-sea derived Streptomyces sp. SCSIO 11594. Mar. Drugs 13, 1304–1316. 10.3390/md13031304 [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Stach J. E. M., Bull A. T. (2005). Estimating and comparing the diversity of marine actinobacteria. Antonie van Leeuwenhoek 87, 3–9. 10.1007/s10482-004-6524-1 [DOI] [PubMed] [Google Scholar]
  59. Sun Y., Takada K., Nogi Y., Okada S., Matsunaga S. (2014). Lower homologues of ahpatinin, aspartic protease inhibitors, from a marine Streptomyces sp. J. Nat. Prod. 77, 1749–1752. 10.1021/np500337m [DOI] [PubMed] [Google Scholar]
  60. Thistle D. (2003). The deep-sea floor: an overview, in Ecosystems of the Deep Ocean, ed Tyler P. A. (Amsterdam: Elsevier; ), 5–39. [Google Scholar]
  61. Tian X. P., Long L. J., Li S. M., Zhang J., Xu Y., He J., et al. (2013). Pseudonocardia antitumoralis sp. nov., a deoxynyboquinone-producing actinomycete isolated from a deep-sea sediment. Int. J. Syst. Evol. Microbiol. 63, 893–899. 10.1099/ijs.0.037135-0 [DOI] [PubMed] [Google Scholar]
  62. Tian X. P., Long L. J., Wang F. Z., Xu Y., Li J., Zhang J., et al. (2012a). Streptomyces nanhaiensis sp. nov., a marine streptomycete isolated from a deep-sea sediment. Int. J. Syst. Evol. Microbiol. 62, 864–868. 10.1099/ijs.0.031591-0 [DOI] [PubMed] [Google Scholar]
  63. Tian X. P., Xu Y., Zhang J., Li J., Chen Z., Kim C. J., et al. (2012b). Streptomyces oceani sp. nov., a new obligate marine actinomycete isolated from a deep-sea sample of seep authigenic carbonate nodule in South China Sea. Antonie van Leeuwenhoek 102, 335–343. 10.1007/s10482-012-9743-x [DOI] [PubMed] [Google Scholar]
  64. Tian X. P., Zhi X. Y., Qiu Y. Q., Zhang Y. Q., Tang S. K., Xu L. H., et al. (2009). Sciscionella marina gen. nov., sp. nov., a marine actinomycete isolated from a sediment in the northern South China Sea. Int. J. Syst. Evol. Microbiol. 59, 222–228. 10.1099/ijs.0.001982-0 [DOI] [PubMed] [Google Scholar]
  65. Ulanova D., Goo K. S. (2015). Diversity of actinomycetes isolated from subseafloor sediments after prolonged low-temperature storage. Folia Microbiol. 60, 211–216. 10.1007/s12223-014-0361-z [DOI] [PubMed] [Google Scholar]
  66. Um S., Kim Y. J., Kwon H., Wen H., Kim S. H., Kwon H. C., et al. (2013). Sungsanpin, a lasso peptide from a deep-sea streptomycete. J. Nat. Prod. 76, 873–879. 10.1021/np300902g [DOI] [PubMed] [Google Scholar]
  67. Vizcaíno A. S., González V., Branã A. F., Molina A., Acunã J. L., Garcıá L. A., et al. (2015). Myceligenerans cantabricum sp. nov., a barotolerant actinobacterium isolated from a deep cold-water coral. Int. J. Syst. Evol. Microbiol. 65, 1328–1334. 10.1099/ijs.0.000107 [DOI] [PubMed] [Google Scholar]
  68. Wagner M., Abdel-Mageed W. M., Ebel R., Bull A. T., Goodfellow M., Fiedler H. P., et al. (2014). Dermacozines H−J isolated from a deep-sea strain of Dermacoccus abyssi from Mariana Trench sediments. J. Nat. Prod. 77, 416–420. 10.1021/np400952d [DOI] [PubMed] [Google Scholar]
  69. Wang Q., Song F. H., Xiao X., Huang P., Li L., Monte A., et al. (2013). Abyssomicins from the south China sea deep sea sediment Verrucosispora sp.: natural thioether michael addition adducts as antitubercular prodrugs. Angew. Chem. Int. Ed. Engl. 52, 1231–1234. 10.1002/anie.201208801 [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Wang W., Cai B., Shao Z. (2014). Oil degradation and biosurfactant production by the deep sea bacterium Dietziamaris As-13-3. Front. Microbiol. 5:711. 10.3389/fmicb.2014.00711 [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Williams S. T., Shameemullah M., Watson E. T., Mayfield C. I. (1972). Studies on the ecology of actinomycetes in soil. VI. The influence of moisture tension on growth and survival. Soil Biol. Biochem. 4, 215–225. 10.1016/0038-0717(72)90014-4 [DOI] [Google Scholar]
  72. Wu Y. H., Wu M., Wang C. S., Wang X. G., Yang J. Y., Oren A., et al. (2008). Microbacterium profundi sp. nov., isolated from deep-sea sediment of polymetallic nodule environments. Int. J. Syst. Evol. Microbiol. 58, 2930–2934. 10.1099/ijs.0.2008/000455-0 [DOI] [PubMed] [Google Scholar]
  73. Xiao J., Luo Y., Xie S., Xu J. (2011a). Serinicoccus profundi sp. nov., an actinomycete isolated from deep-sea sediment, and emended description of the genus Serinicoccus. Int. J. Syst. Evol. Microbiol. 61, 16–19. 10.1099/ijs.0.019976-0 [DOI] [PubMed] [Google Scholar]
  74. Xiao J., Luo Y., Xu J., Xie S., Xu J. (2011b). Modestobacter marinussp. nov., a psychrotolerant actinobacterium from deep-sea sediment, and emended description of the genus Modestobacter. Int. J. Syst. Evol. Microbiol. 61, 1710–1714. 10.1099/ijs.0.023085-0 [DOI] [PubMed] [Google Scholar]
  75. Xu D. B., Ye W. W., Han Y., Deng Z. X., Hong K. (2014). Natural products from mangrove actinomycetes. Mar. Drugs 12, 2590–2613. 10.3390/md12052590 [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Xu Y., Li H., Li X., Xiao X., Qian P. Y. (2009). Inhibitory effects of a branched – chain fatty acid on larval settlement of the polychaete hydroides elegans. Mar. Biotechnol. (NY). 11, 495–504. 10.1007/s10126-008-9161-2 [DOI] [PubMed] [Google Scholar]
  77. Yang X. W., Peng K., Liu Z., Zhang G. Y., Li J., Wang N., et al. (2013a). Strepsesquitriol, a rearranged zizaane-type sesquiterpenoid from the deep-sea-derived actinomycete Streptomyces sp. SCSIO 10355. J. Nat. Prod. 76, 2360–2363. 10.1021/np400923c [DOI] [PubMed] [Google Scholar]
  78. Yang X. W., Zhang G. Y., Ying J. X., Yang B., Zhou X. F., Steinmetz A., et al. (2013b). Isolation, characterization, and bioactivity evaluation of 3-((6-methylpyrazin-2yl)methyl)- 1H-indole, a new alkaloid from a deep-sea-derived actinomycete Serinicoccus profundi sp. nov. Mar. Drugs 11, 33–39. 10.3390/md11010033 [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. You Z. Y., Wang Y. H., Zhang Z. G., Xu M. J., Xie S. J., Han T. S., et al. (2013). Identification of two novel anti-Fibrotic benzopyran compounds produced by engineered strains derived from Streptomyces xiamenensis M1-94P that originated from deep-sea sediments. Mar. Drugs 11, 4035–4049. 10.3390/md11104035 [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Yu J., Zhang L., Liu Q., Qi X. H., Ji Y., Kim B. S. (2015). Isolation and characterization of actinobacteria from Yalujiang coastal wetland, North China. Asian Pac. J. Trop. Biomed. 5, 555–560. 10.1016/j.apjtb.2015.04.007 [DOI] [Google Scholar]
  81. Yu L., Lai Q., Yi Z., Zhang L., Huang Y., Gu L., et al. (2013). Microbacterium sediminis sp. nov., a psychrotolerant, thermotolerant, halotolerant and alkalitolerant actinomycete isolated from deep-sea sediment. Int. J. Syst. Evol. Microbiol. 63, 25–30. 10.1099/ijs.0.029652-0 [DOI] [PubMed] [Google Scholar]
  82. Zhang G., Zhang Y., Yin X., Wang S. (2015). Nesterenkonia alkaliphila sp. nov., an alkaliphilic, halotolerant actinobacteria isolated from the western Pacific Ocean. Int. J. Syst. Evol. Microbiol. 65, 516–521. 10.1099/ijs.0.065623-0 [DOI] [PubMed] [Google Scholar]
  83. Zhang L., Xi L., Ruan J., Huang Y. (2012). Microbacterium marinum sp. nov., isolated from deep-sea water. Syst. Appl. Microbiol. 35, 81–85. 10.1016/j.syapm.2011.11.004 [DOI] [PubMed] [Google Scholar]
  84. Zhang Q., Li S., Chen Y., Tian X., Zhang X., Zhang G., et al. (2013). New diketopiperazine derivatives from a deep-sea-derived Nocardiopsis alba SCSIO 03039. J. Antibiot. 66, 31–36. 10.1038/ja.2012.88 [DOI] [PubMed] [Google Scholar]
  85. Zhang W. J., Liu Z., Li S. M., Yang T. T., Zhang Q. B., Ma L., et al. (2012). Spiroindimicins A-D: new Bisindole alkaloids from a deep-sea-derived actinomycete. Org. Lett. 14, 3364–3367. 10.1021/ol301343n [DOI] [PubMed] [Google Scholar]
  86. Zhang W. J., Ma L., Li S. M., Liu Z., Chen Y. C., et al. (2014). Indimicins A-E, Bisindole alkaloids from the deep-sea-derived Streptomyces sp. SCSIO 03032. J. Nat. Prod. 77, 1887–1892. 10.1021/np500362p [DOI] [PubMed] [Google Scholar]
  87. Zhang W., Li S., Zhu Y., Chen Y., Chen Y., Zhang H., et al. (2014). Heronamides D-F, polyketide macrolactams from the deep-sea-derived Streptomyces sp. SCSIO 03032. J. Nat. Prod. 77, 388–391. 10.1021/np400665a [DOI] [PubMed] [Google Scholar]
  88. Zhou X., Huang H. B., Li J., Song Y. X., Jiang R. W., Liu J., et al. (2014). New antiinfective cycloheptadepsipeptide congeners and absolute stereochemistry from the deep sea-derived Streptomyces drozdowiczii SCSIO 10141. Tetrahedron 70, 7795–7801. 10.1016/j.tet.2014.02.007 [DOI] [Google Scholar]
  89. Zhu Y., Zhang W., Chen Y., Yuan C., Zhang H., Zhang G., et al. (2015). Characterization of heronamide biosynthesis reveals a tailoring hydroxylase and indicates migrated double bonds. Chembiochem 16, 2086–2093. 10.1002/cbic.201500281 [DOI] [PubMed] [Google Scholar]

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