Skip to main content
NCBI home page
Poultry Science logoLink to Poultry Science
. 2024 Feb 16;103(4):103562. doi: 10.1016/j.psj.2024.103562

Exploring the modulatory effects of brown seaweed meal and extracts on intestinal microbiota and morphology of broiler chickens challenged with heat stress1

Fisayo Oretomiloye *, Deborah Adewole *,†,2
PMCID: PMC10909895  PMID: 38417338

Abstract

Brown seaweed (Ascophyllum nodosum) is known for its prebiotic roles and can improve animal intestinal health by enhancing the growth of beneficial microbes and inhibiting pathogenic ones. However, the gut health-modulatory roles of brown seaweed on chickens challenged with heat stress (HS) are rarely studied. The current study examined the effects of brown seaweed meal (SWM) and extract (SWE) on the ceca microbiota and small intestinal morphology of chickens challenged or unchallenged with HS. Three hundred and thirty-six 1-day-old Ross 308 broiler chicks were randomly assigned to either a thermoneutral (TN; 24 ± 1°C); or HS room (HS; 32–34°C, 8 h/d from d 21 to 27). All birds in each room were randomly allotted to 4 treatments – control (CON), CON + 1 mL/L seaweed extract (SWE) in drinking water, CON + 2 mL/L SWE in drinking water, and CON + 2% seaweed meal (SWM) in feed and raised for 28 d. On d 14 and 28, 12 and 24 birds per treatment group, respectively, were euthanized to collect the ceca content for gut microbiota analysis and small intestinal tissues for morphological examination. On d 14, 2% SWM increased (P = 0.047) the relative abundance of cecal Fecalibacterium and all brown seaweed treatments improved jejunal villus height (VH) and VH:CD compared to the CON diet. On d 28, HS significantly reduced (P < 0.05) ileal VH, VW, and VH:CD, and duodenal VH and VH:CD. Among the HS group, 2% SWM and 2 mL/L SWE significantly increased (P < 0.05) the relative abundance of Lactobacillus, Sellimonas, and Fournierella, compared to the CON diet. HS birds fed with 2% SWM had higher ileal VH and VH:CD compared to other treatments. In summary, SWM and SWE enhanced the abundance of beneficial microbes and improved small intestinal morphology among HS chickens. This implies that seaweed could potentially alleviate HS-induced intestinal impairment in chickens.

Key words: brown seaweed, heat stress, cecal microbiota, intestinal morphology, broiler chicken

INTRODUCTION

Heat stress continues to pose a serious threat to the poultry industry, particularly with the increase in the environmental temperature globally (Ahmad et al., 2022). Heat stress has wide-ranging implications on the general welfare, health, and productivity of chickens. Several studies have highlighted the profound effects of heat stress on the gut health of broiler chickens (Quinteiro-Filho et al., 2010, 2012; Shi et al., 2019; Goel et al., 2023). Heat stress can alter gut microbiota, which can negatively affect growth performance and disease resistance in chickens, subsequently reducing production efficiency (Rinttila and Apajalahti, 2013). Shi et al. (2019) showed that heat stress changed the gut microbiota composition of chickens, resulting in a higher proportion of Tenericutes and Proteobacteria and a lower proportion of Bacteroidetes and Cyanobacteria. Heat stress can also impair the intestinal morphology of chickens (Nanto-Hara et al., 2020) in relation to reduced villus height, villus surface area and intestinal weight (Abdelqader and Al-Fataftah, 2016). Given the adverse effects of heat stress, several ameliorative strategies, including genetics, housing, management strategies and nutritional approaches, have been proposed to alleviate heat stress (Kumari and Nath, 2018; Vandana et al., 2021). However, mitigative approaches such as housing and management continue to face shortcomings ranging from high equipment and maintenance costs to lack of constant electricity supply, especially in the tropics (Sumanu et al., 2022). Nutritional supplementation with bioactive substances that possess antioxidant properties seems to be a promising approach for mitigating heat stress in chickens (Arain et al., 2018; Ayo and Ogbuagu, 2021).

Algae are a rich source of antioxidants and contain several bioactive polysaccharides such as fucoidan and laminarin, carotenoids and amino acids that are beneficial to animal and human health (Holdt and Kraan et al., 2011; Agregán et al., 2018; Ferreira et al., 2021; Michalak et al., 2022). They can exert various biological activities including immunomodulatory, antioxidative, antibacterial, hepatoprotective and anti-inflammatory properties (Park et al., 2015; Patel et al., 2021). Some studies have investigated the use of macro and microalgae in poultry production due to their nutritional composition and their biological activities (Coudert et al., 2020; Akinyemi and Adewole, 2022; Liu et al., 2022a; Mishra et al., 2023). Among these, microalgae such as Spirulina platensis have shown promising results by improving growth performance (final body weight), gut morphology parameters and increasing volatile fatty acid-producing genus bacteria in heat-stressed chickens (Chaudhary et al., 2023). Attia et al. (2023) found that Spirulina platensis improved the survival rate and European production efficiency index of chickens exposed to heat stress. Dietary supplementation of microalgae (Spirulina platensis) further improved the gut morphology, enhanced intestinal lactobacilli, and reduced the coliform contents of heat-stressed chickens (Attia et al., 2023). Dietary supplementation of 1,000 mg/kg algae-derived polysaccharides extracted from green seaweed (E. prolifera) tended to increase the duodenal villus height and width and decrease the apoptosis rate of broilers challenged with heat stress (Liu et al., 2021). Our previous study reported the brown seaweed (Ascophyllum nodosum) meal and extract improved the growth performance of broiler chickens irrespective of the HS conditions (Akinyemi and Adewole, 2022). Recently, Archer et al. (2023) found out that Ascophyllum nodosum extract at 0.5 kg/metric ton did not affect growth or feed conversion but could improve the welfare of poultry during heat stress.

Dietary supplementation of 500 and 1,000 ppm Ascophyllum nodosum extract to chicks significantly reduced Camphylobacter jejuni quantities in the chicks’ cecum (Sweeney et al., 2016). The inclusion of 5 to 10 g/kg seaweed blend (green, brown, and red seaweeds) in chickens’ diet also increased the abundance of Firmicutes and Actinobacteria in the ceca (Mohammadigheisar et al., 2020). In vitro investigations revealed that 10 g/kg Ascophyllum nodosum reduced the abundance of Escherichia coli load in the pig stomach and small intestine but enhanced Lactobacilli:Escherichia coli ratio in the small intestine, which indicates the beneficial effects of seaweed on the microbial flora of the animal (Dierick et al., 2009). Owing to the gut health modulatory roles and other biological activities of brown seaweed in chickens, our current study was conducted to test the hypothesis that dietary supplementation of brown seaweed meal and extract will enhance gut health in broiler chickens exposed to heat stress. The specific objectives were to examine the effects of brown seaweed meal (SWM) and extract (SWE) on the ceca microbiota and gut morphology of chickens challenged with heat stress.

MATERIALS AND METHODS

Experimental Design, Management, Housing, and Diets

The experimental procedures were approved by Dalhousie University Animal Use and Care Committee (Ethical code 2021-029), and all chickens were handled according to the Canadian Council on Animal Care (CCAC, 2009) guidelines. The management of birds, housing, experimental designs, seaweeds and experimental diets composition were discussed in the first part of this study (Akinyemi and Adewole, 2022). A total of 336 one-day-old mixed-sex Ross 308 broiler chicks (initial average weight: 39.3g) were obtained from Atlantic Poultry Incorporated, Port Williams, Nova Scotia. Birds were raised in a 2-tier battery cage system at a stocking density of 0.076 m2/birds for 28 d. All treatment groups were evenly distributed across both tiers of the cages. At the room level, the lighting was set to generate 18 h of light and 6 h of darkness, and illumination was slightly reduced from 20 lux to 5 lux from d 0 to 28. Temperature and relative humidity were consistently checked and recorded using Extech Instruments (Nashua, NH) in the 2 experimental rooms. The experiment was conducted during the winter season (February to March) and is a 4 × 2 factorial design; with 2 thermal-controlled rooms; 1) Thermoneutral (TN; 24°C ± 1 on d 21–27), Heat stress (HS; 32–34°C for 8 h/d on d 21–27) and 4 treatments: 1) Corn-wheat-soybean based diet negative control (CON); 2) CON + 1 mL/L seaweed extract in drinking water (1 mL/L SWE), 3) CON + 2 mL/L seaweed extract in drinking water (2 mL/L SWE), and 4) CON + 2% seaweed meal in feed (2% SWM). Water treatment was conducted daily to ensure consistency in the application of seaweed extract. The seaweed extract was mixed daily to maintain the freshness and efficacy of the seaweed extract. Drinking water supplemented with or without seaweed extract was provided in nipple drinkers connected to fabricated water jars from d 0 to 28. To prevent microbial growth and contamination, leftover water was discarded, and the drinking containers were cleaned frequently. The seaweed extract was observed to be completely soluble in water. The in-feed treatment (2% SWM) and the CON were provided with regular water without any seaweed extract. The brown seaweed meal and extract were administered to the chickens from d 0 to 28.

Heat Stress Protocol

The chickens were challenged with HS for 8 h daily from d 21 to 27. The temperature in the HS room steadily increased at 9 am, then 28°C by 10 am, and further raised to 32°C by 12 pm. The temperature was maintained at 34 ± 1°C from 12 pm to 4 pm, then gradually decreased to 28°C by 5 pm and dropped to thermoneutral [TN (24°C ± 1)] for the rest of the day. TN birds were raised at a constant temperature of 24°C ± 1 during the HS period. The TN and HS conditions were regulated by an automatic temperature control system and monitored twice daily. Relative humidity was maintained at <40% for the TN and HS rooms.

Sample Collection

On d 14 and 28, one bird/cage (6 replicates per treatment group) and 2 birds per cage (12 replicates per treatment group), respectively, were randomly selected and euthanized, and the ceca contents were collected, then stored in RNAse and DNAse-free microcentrifuge tubes, placed in liquid nitrogen, followed by storage at −80°C for further microbiota analysis. Intestinal tissues (duodenum, jejunum, and ileum) were also collected and fixed in formalin for morphological examination.

Gut Morphology

The intestinal tissues were harvested from 12 birds per treatment group on d 14, and 24 birds per treatment group on d 28. All samples were processed using the same procedure as described by Oladokun et al. (2021). After sample collection, the intestinal tissues were fixed, embedded in paraffin, sliced into sections (0.5 μm thick), and then stained with hematoxylin and eosin for morphological analysis. The small intestinal morphology slides were visualized using microscope and processed using Leica application (Leica DC480; Leica Microsystems Imaging Solutions Ltd., Concord, ON, Canada). Upon examination, the villus height was measured first; from the base of the intestinal mucosa to the tip of the villus excluding the crypt, then we measured the villus width (halfway between the base and the tip), and crypt depth was measured from the base upward to the region of transition between the crypt and villi. The villus height:crypt depth was then calculated. To ensure the reliability of data, ten morphometric measurements were evaluated per slide by the same individual. On d 28, 960 villi (10 villi/slide) were analyzed per section (duodenum, jejunum, and ileum) while 480 (10 villi/slide) villi were analyzed on d 14. Villi and crypts were selected based on their clear visibility and well-oriented positioning.

DNA Extraction and Sequencing

DNA was extracted from the cecal samples using QIAamp PowerFecal Pro DNA Kit (Cat. No./ID: 51804; Qiagen, Hilden, Germany). Frozen ceca digesta contents were briefly thawed at room temperature before DNA extraction per the manufacturer's protocol. For each sample, 250 mg digesta content was added into PowerBead Pro Tubes, and the subsequent extraction steps were carried out following the company procedures. DNA concentrations and purity were checked using a Nanodrop spectrophotometer (Nanodrop ND1000, Thermo Scientific, Waltham, MA). The A260/280 ratio for the DNA samples falls within the range of 1.8 to 2.0, which is indicative of high-quality DNA and the absence of inhibitors (Supplementary Table 1). The DNA samples (concentration; 10–200 ng/µL) were later shipped on an ice pack to the Integrated Microbiome Resource (http://imr.bio) of Dalhousie University where sequencing was carried out. PCR was performed to amplify with dual-barcoded primers targeting the Bacteria-specific V3–V4 region (341F = 5′-CCTACGGGNGGCWGCAG-3′ and 805R = 3′-GACTACHVGGGTATCTAATCC-5′) of the bacterial 16S rRNA genes (Klindworth et al., 2013) at the Integrated Microbiome Resource, Dalhousie University.

Data Analysis

The ceca microbiota relative abundance and small intestinal morphology dataset were subjected to analysis of variance (ANOVA) using a General Linear Model of Minitab LLC (2019) software. Values were considered statistically significant at P ≤ 0.05. Microbiome Helper pipeline (https://github.com/LangilleLab/microbiome_helper/wiki), was used to analyzed the ceca microbiota, based on Quantitative Insights Into Microbial Ecology 2 (QIIME 2). Primer sequences were trimmed from sequencing reads and implemented into QIIME2 (Bolyen et al., 2019). Taxonomic assignment was performed with the SILVA database 123 and other bioinformatics steps were followed as highlighted in Oladokun et al. (2022) and Erinle et al. (2023). We used rarefaction curves to examine the alpha diversity for all samples. The relative abundance of the bacteria was visualized using stacked bar charts at different levels. Functional gene prediction was determined using Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) (Langille et al., 2013).

RESULTS

Cecal Microbial Composition and Diversity

The relative abundance of the predominant bacteria phyla and genus in the ceca of broiler chickens raised for 14 d are presented in Figure 1. On d 14, four (4) phyla and sixty-nine (69) genera existed in the ceca of broiler chickens. At the phyla level, the dominant bacteria observed across all the dietary treatments were Firmicutes (range of 99.41–99.57%), Proteobacteria (range of 0.13–0.40%), Actinobacteria (0.09–0.32%), with a lesser amount of Bacteroidota (0–0.02%). 2% SWM reduced the proportion of proteobacteria by 63.8% and increased the proportion of Actinobacteriota by 39.1% compared to CON. We found the presence of Bacteroidota among chickens that received 2% SWM and 1 mL/L SWE only, though in low proportion. At the genus level, the most predominant bacteria across different dietary treatments on d 14 were Streptococcus, Fecalibacterium, Lactobacillus, Ruminococcus_torques, Blautia, Romboutsia, Subdoligranulum, Butyricicoccus, Eubacterium_coprostanoligenes, and Anaerotruncus (Figure 1). The most abundant microbes among the chickens treated with 1 ml/L SWE, 2 ml/L SWE and 2% SWM were Lactobacillus, Streptococcus, and Fecalibacterium, respectively. Considering the top 10 abundant microbes, the dietary treatments did not have significant effect on the abundance of cecal microbes, aside from Fecalibacterium. 2% SWM significantly increased (P = 0.047) Fecalibacterium in the ceca of broiler chickens compared to the control, while the effects of 1and 2 ml/L SWE on the abundance of Fecalibacterium were intermediate (Figure 1). The effect of dietary supplementation of the brown seaweed products on cecal microbial diversity on d 14 is shown in Figure 1D. Alpha diversity accessed by Shannon indices on d 14 and 28 were not affected by the challenge model (Figure 1D and 2D).

Figure 1.

Figure 1

Open in a new tab

(A) Relative abundance of the predominant phyla group across all treatments on day 14. (B) Relative abundance of the predominant genera across all treatments on d 14. (C) Effect of treatments on the abundance of Fecalibacterium. (D) Alpha diversity accessed by Shannon index on d 14. Treatments include CON (corn-soybean meal-wheat–based diet), 1 mL/L SWE (chicks supplied brown seaweed extract in drinking water at 1 mL/L), 2 mL/L SWE (chicks supplied brown seaweed extract in drinking water at 2 mL/L), 2% SWM (chicks fed CON + 2% brown seaweed in feed). a, b, cmeans assigned different lowercase superscript letters are significantly different, P < 0.05 (Tukey's procedure).

Figure 2.

Figure 2

Open in a new tab

(A) Relative abundance of the predominant phyla group across all treatments on day 28 irrespective of heat stress. (B) Relative abundance of the predominant genera across all treatments on day 28 irrespective of heat stress. (C) Effects of heat stress on the relative abundance of predominant phyla on day 28. (D) Alpha diversity accessed by Shannon index on day 28 irrespective of heat stress. Treatments include CON (corn-soybean meal-wheat–based diet), 1 ML/L SWE (chicks supplied brown seaweed extract in drinking water at 1 mL/L), 2 mL/L SWE (chicks supplied brown seaweed extract in drinking water at 2 mL/L), 2% SWM (chicks fed CON + 2% brown seaweed in feed). a, b, cmeans assigned different lowercase superscript letters are significantly different, P < 0.05 (Tukey's procedure).

The d 28 relative abundance of the predominant bacteria phyla and genera in the ceca of broiler chickens are shown in Figure 2. On d 28, 4 phyla and 96 genera were observed irrespective of heat stress challenge. The ceca microbiota phyla taxa on d 28 showed a similar trend as that of d 14, as the relative abundance of Firmicutes (range of 99.1–99.68%) was higher than Proteobacteria (range of 0.10–0.56%), and Actinobacteria (range of 0.10–0.39%) across the treatment groups. There was no significant interaction on the composition of the ceca microbiota phyla. Heat stress significantly reduced the relative abundance of Firmicutes (P < 0.001) and Actinobacteria (P < 0.001) compared to the broilers raised in the TN zone (Figure 2C). At the genus level, heat stress significantly increased (P < 0.05) Marvinbryantia, Shuttleworthia, Anaerotruncus, Erysipelotrichaceae and decreased Eubacterium Coprostanoligenes group, Anaerofilum, Flavonifractor, Ruminococcus and Incertae sedis (Figure 3). Among the heat stress group, 2% SWM and 2 mL/L SWE significantly increased the relative abundance of Lactobacillus, Sellimonas, Anaerofustis and Fournierella compared to the CON (Figure 3).

Figure 3.

Figure 3

Open in a new tab

(A) Significant differences in microbes between chickens raised under thermoneutral (T) and heat stress (H) conditions on day 28. (B) Differently enriched genera among heat-stressed birds fed with brown seaweed meal and extract. Treatments include BASAL _HEATSRESSED (heat-stressed birds fed with corn-soybean meal-wheat–based diet), 2 ml_ SWE_HEATSTRESSED (heat-stressed chicks supplied with brown seaweed extract in drinking water at 2 ml/L), 2percent_SWM_HEATSTRESSED (heat-stressed chicks fed with 2% brown seaweed in feed).

Predicted Functions of Ceca Microbiota

On microbial functional profiles, 2% SWM differentially reduced the abundances of functional pathways related to L-tryptophan biosynthesis (Trpsyn), riboflavin synthesis (RIBOSY), L-ornithine biosynthesis I (GLUTORN-PWY), arginine and polyamine synthesis (Arg+polyamine-syn) and polyamine-synthesis on d 14, compared to 2 mL/L SWE and control diet (supplementary figure 1). On d 28, 2% SWM enhanced L-methionine biosynthesis, L-methionine biosynthesis I and I I I (PWY-5347, HOMOSER-METSYN-PWY, HSERMETANA-PWY), thiazole component of thiamine diphosphate biosynthesis I (PWY-6892, 6891), glycogen degradation (GLYCOCAT-PWY), TEICHOICACID-PWY, superpathway of coenzyme A biosynthesis I (PANTOSYN-PWY), thiamine biosynthesis (THISYN-PWY) but reduced sucrose degradation (PWY-5384), compared to the control diet among the heat-stressed chickens. 2 ml/L SWE enriched the biosynthesis of peptidoglycan (PWY-6470), gluconeogenesis pathway (GLUCONEO-PWY), and incomplete reductive TCA cycle (P42-PWY) but reduced N-acetylneuraminate degradation (P441-PWY), compared to the control diet. (Figure 4).

Figure 4.

Figure 4

Open in a new tab

Differently enriched pathways among heat-stressed birds fed with brown seaweed meal and extract. Treatments include BASAL _HEATSRESSED (heat-stressed birds fed with corn-soybean meal-wheat–based diet;)), 2 ml_ SWE_HEATSTRESSED (heat-stressed chicks supplied with brown seaweed extract in drinking water at 2 ml/L), 2percent_SWM_HEATSTRESSED (heat-stressed chicks fed with 2% brown seaweed in feed).

Small Intestinal Morphology

The effects of brown seaweed meal and extract on the intestinal morphology of broiler chickens on d 14, before the heat stress challenge, is presented in Table 1. The inclusion of brown seaweed meal and extract significantly affected the duodenal and jejunal morphology. Drinking water supplemented with 2 ml/L SWE significantly reduced (P < 0.001) the duodenal VH compared to other treatments. A total of 2% SWM significantly improved (P = 0.010) the VW, compared to the control diet, while the 1 mL/L SWE and 2 mL/L SWE were intermediate between the 2% SWM and the control diet. A total of 2 mL/L SWE improved the duodenal CD (P < 0.001) and VH:CD (P = 0.014), compared to the other treatment groups. In the jejunum, 1 mL/L SWE, 2 mL/L SWE, and 2% SWM significantly improved (P < 0.001) VH and VH:CD, compared to the control diet.

Table 1.

Effects of brown seaweed on the gut morphology of broiler chickens raised for 14 d.

Parameters Treatment1
 SEM2 P value
CON 1 mL/L SWE 2 mL/L SWE 2% SWM
Duodenum
Villus height (mm) 1.61a 1.65a 1.50b 1.69a 0.015 <0.001
Villus width (mm) 0.17b 0.18ab 0.19ab 0.20a 0.003 0.010
Crypt depth (mm) 0.14b 0.16a 0.12c 0.15ab 0.002 <0.001
VH:CD 11.7ab 10.3b 12.0a 11.0ab 0.208 0.014
Jejunum
Villus height (mm) 0.71b 0.81a 0.79a 0.82a 0.008 <0.001
Villus width (mm) 0.18bc 0.17c 0.20ab 0.22a 0.004 <0.001
Crypt depth (mm) 0.106ab 0.105ab 0.10b 0.109a 0.001 0.042
VH:CD 6.53b 7.62a 7.86a 7.40a 0.126 <0.001
Ileum
Villus height (mm) 0.42 0.46 0.47 0.45 0.009 0.217
Villus width (mm) 0.20 0.20 0.21 0.21 0.005 0.562
Crypt depth (mm) 0.09 0.09 0.09 0.09 0.004 0.532
VH:CD 4.42 5.16 5.27 5.00 0.127 0.084
Open in a new tab
a, b, c

In a row, least square means assigned different lowercase superscript letters are significantly different, P < 0.05 (Tukey's procedure).

1

Treatment includes CON (control (corn-soybean meal-wheat–based diet;)), 1 mL/L SWE (chicks supplied brown seaweed extract in drinking water at 1 mL/L), 2 mL SWE (chicks supplied brown seaweed extract in drinking water at 2 mL/L), 2% SWM (chicks fed CON + 2% brown seaweed in feed).

2

SEM = Standard error of means.

Further result on the effects of brown seaweed meal and extract on the small intestinal morphology of broiler chickens challenged with heat stress (d 28) is presented in Table 2. There was a significant interaction between the dietary treatments and challenge model on duodenal VW (P = 0.008), CD (P = 0.012), VH:CD (P = 0.002), jejunal VH (P < 0.001), ileal VH (P < 0.001), VW (P = 0.006), CD (P = 0.002), and VH:CD (P = 0.001). Heat stress significantly reduced duodenal VH (P = 0.003), VH:CD (P = 0.004), jejunal CD (P = 0.010), and ileal VH (P < 0.001), VW (P = 0.040), and VH:CD (P = 0.004). In the duodenal section,1 ml/L SWE significantly improved VH (P = 0.010) and VH:CD (P = 0.004) among the heat-stressed challenged birds compared with the control diet. The ileal morphology result showed that the dietary supplementation of 2% SWM significantly improved (P < 0.001) VH:CD among heat-stressed birds compared with other treatments. A total of 2% SWM and 2 mL/L SWE improved (P < 0.001) the VH, while 1 mL/L and 2 mL/L SWE improved (P = 0.003) the VW of broiler chickens challenged with heat stress compared with other treatments. Representative ileal histology images based on treatments are presented in Supplementary Figure 2.

Table 2.

Effects of brown seaweed on the gut morphology of broiler chickens challenged with heat stress (d 28).

Parameters Thermoneutral
 Heat stress
 Temperature
 SEM3 P value
CON 1 mL/L SWE 2 mL/L SWE 2% SWM CON 1 mL/L SWE 2 mL/L SWE 2% SWM TN1 HS2 Diet Temp Diet × Temp.
Duodenum
Villus height (mm) 1.87c 2.14a 2.01b 2.07ab 1.92b 2.05a 1.93b 1.97ab 2.03a 1.97b 0.011 <0.001 0.003 0.069
Villus width (mm) 0.23ab 0.24a 0.22b 0.24ab 0.22 0.21 0.23 0.22 0.23 0.22 0.003 0.962 0.094 0.008
Crypt depth (mm) 0.139a 0.135ab 0.12b 0.13ab 0.14ab 0.13b 0.13ab 0.14a 0.13 0.13 0.003 0.044 0.153 0.012
VH:CD 13.4b 15.7a 16.1a 16.0a 13.7b 15.59a 14.3ab 13.6b 15.2a 14.3b 0.159 <0.001 0.004 0.002
Jejunum
Villus height (mm) 1.02c 1.09bc 1.15b 1.24a 1.09 1.11 1.09 1.12 1.13 1.10 0.007 <0.001 0.118 <0.001
Villus width (mm) 0.24a 0.21b 0.24a 0.22ab 0.23 0.23 0.23 0.23 0.23 0.23 0.002 0.064 0.994 0.076
Crypt depth (mm) 0.10 0.10 0.10 0.10 0.10 0.10 0.09 0.09 0.01a 0.096b 0.001 0.311 0.010 0.221
VH:CD 10.5b 10.7b 11.4ab 12.5a 11.0 11.1 11.6 11.7 11.3 11.6 0.107 <0.001 0.140 0.124
Ileum
Villus height (mm) 0.58 0.61 0.55 0.59 0.49b 0.48b 0.62a 0.67a 0.61a 0.55b 0.011 <0.001 <0.001 <0.001
Villus width (mm) 0.21ab 0.23a 0.20b 0.21ab 0.19b 0.22a 0.22a 0.20ab 0.21a 0.20b 0.004 0.010 0.040 0.006
Crypt depth (mm) 0.11a 0.10ab 0.09b 0.10ab 0.10a 0.09b 0.10a 0.097ab 0.10 0.10 0.002 0.054 0.253 0.002
VH:CD 5.48 6.15 6.09 6.07 4.73c 5.36bc 5.89b 6.78a 6.10a 5.64b 0.123 <0.001 0.004 0.001
Open in a new tab

Abbreviation: Temp., temperature.

a, b, c

In a row, least square means assigned different lowercase superscript letters are significantly different, P < 0.05 (Tukey's procedure).

Treatment includes CON (control (corn-soybean meal-wheat–based diet;)), 1 ml/L SWE (chicks supplied brown seaweed extract in drinking water at 1 ml/L), 2 ml SWE (chicks supplied brown seaweed extract in drinking water at 2 mL/L), 2% SWM (chicks fed CON + 2% brown seaweed in feed).

1

HS: heat stress.

2

TN: thermoneutral.

3

SEM = standard error of means.

DISCUSSION

Despite years of research, heat stress continues to negatively impact the welfare, productivity, and health of broiler chickens (Rostagno, 2020). The negative effects of heat stress on broiler chickens’ growth performance and blood parameters have been reported in the part 1 of this study (Akinyemi and Adewole, 2022). Heat stress reduced average feed intake and plasma enzymatic antioxidants but increased rectal temperature, serum IgG and IgM and some blood parameters (sodium, chloride, uric acid, amylase) (Akinyemi and Adewole, 2022). One of the main physiological effects of heat stress is the impairment of the gastrointestinal tract which plays a major role in nutrient digestion and absorption (Kogut et al., 2017; Wang et al., 2021a). Heat stress can alter gastrointestinal tract functions by reducing blood flow, increasing intestinal permeability, disrupting the intestinal barrier, and causing dysbiosis (Gupta et al., 2017; Rostagno, 2020). On the other hand, brown seaweed can exert beneficial effects on the gut health of chickens raised under thermoneutral conditions by increasing the abundance of beneficial microbes and reducing pathogenic ones (Sweeney et al., 2016; Mohammadigheisar et al., 2020). Existing studies on heat-stressed chickens and brown seaweed (Ascophyllum nodosum) mainly focused on growth performance, stress indicators, and blood parameters (Archer et al., 2023; Akinyemi and Adewole, 2022; Borzouie et al., 2020) and excluded intestinal health parameters. Our current study postulates new findings on brown seaweed's potential to enhance the intestinal health of heat-stressed birds.

On cecal microbiota composition, Firmicutes, Proteobacteria and Actinobacteria are the dominating phyla in the current study which is in accordance with our previous studies on broiler chickens (Erinle et al., 2023; Oladokun and Adewole, 2023). Considering the effects of dietary treatments on the genus, 2% SWM treatment increased the relative abundance of cecal Fecalibacterium (60.5%) compared to the control diet (3.6%) on d 14, but no treatment effects on d 28. Our result implies that brown seaweed can stimulate the growth of Fecalibacterium by providing fermentable substrates such as polysaccharides. In vitro studies have demonstrated that seaweeds have the potential to increase the abundance of Fecalibacterium (Kong et al., 2021; Charoensiddhi et al., 2022). He et al. (2021) suggested that Fecalibacterium prausnitzii, a major specie of the Fecalibacterium genus, may have a potential as a next-generation probiotic, capable of reducing intestinal inflammation and promoting gut health in the host. In terms of abundance, a lower presence of this species has been linked to chronic inflammatory diseases, while higher levels have been found to offer protective effects against such conditions (He et al., 2021). Fecalibacterium plays a crucial role in the production of butyric acid, a compound that facilitates the degradation of polysaccharides (Charoensiddhi et al., 2017). Research studies have indicated a positive correlation between Fecalibacterium and acetic acid production (Zhu et al., 2022; Gu et al., 2023) and its roles have been extensively investigated in various studies. For instance, Sokol et al. (2008) reported that Fecalibacterium equipoised dysbiosis and demonstrated anti-inflammatory effects on the cellular and immune response in humans by producing metabolites that modulated the expression of inflammatory genes and cytokines (Sokol et al., 2008). Additionally, Fecalibacterium has been found to prevent hepatic damage in mouse models (Shin et al., 2023) and has been associated with total cholesterol and low-density lipoprotein cholesterol, which are considered biomarkers for heart diseases (Xu et al., 2021). However, the adaptation of the chickens to the seaweed diet may result in the cecal microbiota reaching a new equilibrium, where other bacteria strains compete with Fecalibacterium for available nutrients. The microbiota of chickens tends to stabilize and exhibit less variation as they mature due to the acquisition and replacement of new bacterial strains (Takeshita et al., 2021). This might probably explain the observed differences in the relative abundance of Fecalibacterium on days 14 and 28.

Further results from our current study showed that heat stress reduced the relative abundance of Anaerofilum, Flavonifractor, Ruminococcus and Incertae sedis. The observed changes may impair the gut health and immune function of the broiler chickens considering their involvement in carbohydrate utilization and immune modulation (Wang et al., 2019; Liu et al., 2022b). Previous studies have reported that Ruminococcus plays an essential role in the conversion and degradation of complex polysaccharides into nutrients for their hosts (La Reau and Suen, 2018). The reduction in the relative abundance of Ruminococcus could increase the risk of cardiovascular diseases in humans (Lakshmanan et al., 2022). In addition, Flavonifractor can metabolize catechin in the gut and help in alleviating antigen-induced Th2 immune responses (Ogita et al., 2020).

Among the heat stress group, brown seaweed treatments (2% SWM, and 1 and 2 mL/L SWE) enhanced the relative abundance of Lactobacillus, Sellimonas, Fournierella and Anaerofustis compared to the control diet. Seaweed inclusion has been shown to increase Lactobacillus spp. counts (Balasubramanian et al., 2021), which can reduce the absorption of toxins from the chicken gut (Jahromi et al., 2017). Lactobacilli are excellent butyrate producers that can enhance acetic and lactic acid, eliminating pathogenic infection and thus improving growth performance (Song et al., 2018). Lactic acid bacteria can impede the growth of pathogenic bacteria by reducing pH and enhancing bacteriocins, which can increase the concentrations of blood immunoglobulins (Kim et al., 2018). Liu et al. (2023) validated the bacteria Fournierella for its immunomodulatory abilities and established their involvement in the maintenance of intestinal homeostasis in chickens. A positive correlation between the presence of genus Fournierella and the increase in body weight in broiler chickens has been previously shown (Farkas et al., 2022). Similarly, the genus Selimonas showed a significant correlation with residual feed intake in ducks, which may have resulted in enhanced energy availability for body growth owing to its involvement in carbohydrate metabolism (Bai et al., 2023). Selimonas also exhibited a positive effect on restoring intestinal balance following dysbiosis occurrence (Muñoz et al., 2020).

Anaerofustis is a member of the Eubacteriaceae family, a gram-positive bacterium, and has been found in the gut of humans and animals (Finegold et al., 2004; Feng et al., 2022). Genus Anaerofustis plays a beneficial role in the gut microbiota due to its involvement in the production of butyrate, a short-chain fatty acid with anti-inflammatory and immunomodulatory properties (Wang et al., 2021b; Njoku et al., 2023) and is enriched in animals fed carbohydrate-rich diets (Xiang et al., 2021; Goel et al., 2022). The presence of Anaerofustis in the intestine was associated with enhanced degradation of dietary fibers and synthesis of short-chain fatty acids, which might enhance the antioxidant capacity and morphological integrity of the gut epithelium (Wang et al., 2022). Hence, the increase in the abundance of these 4 beneficial genera despite the heat stress challenge indicates that brown seaweed can mitigate heat stress-impaired ceca microbiota balance.

The functional predicted analysis by PICRUSt showed that 2% SWM had a significant effect on biosynthesis and degradation in broiler chickens. L-methionine biosynthesis, which was mostly enriched in chickens fed with 2% SWM, was previously associated with growth performance in piglets (Jiao et al., 2023). Methionine is an essential amino acid that participates in several biological processes, such as DNA methylation, protein structure, and polyamine synthesis (Cavuoto and Fenech 2012). The metabolism of methionine through the transmethylation pathway generates S-adenosylmethionine, which is important for the methylation of lipids, and proteins (Dash et al., 2016). Hu et al. (2022) found that methionine restriction altered the microbial community balance and functions, while methionine supplementation enhanced the stability of gut microbiota and lipid metabolism of fish. According to Lee et al. (2021), heat-stressed chicks fed with L-Methionine had reduced intestinal blood vessel formation and maintained normal glucose and lipid metabolism. The enhancement of L-methionine biosynthesis in this study suggests that seaweed can protect chickens from stress-induced effects. A total of 2% SWM also enriched pathways responsible for the synthesis of thiamine diphosphate biosynthesis and teichoicacid-pwy. Thiamin diphosphate is a well-known thiamin compound because of its role as an enzymatic cofactor (Bettendorff and Wins 2009). Thiamine deficiency in chickens can result in reduced feed intake and body weight, and it is a sign of cardiologic and neurologic impairment (Burgos et al., 2006). Increased activity of thiamine pyrophosphate-dependent enzymes will cause over flux of carbohydrate oxidation via the tricarboxylic acid cycle and pentose phosphate pathway (Kamarudin et al., 2017). Teichoicacid-pwy have crucial roles in cellular proliferation, environmental stress resistance, and host colonization and infection (Van Dalen et al., 2020). Seaweed extract at 2 ml/L inclusion increased the pathway of gluconeogenesis, TCA and peptidoglycan among heat-stressed birds in our study. Metabolic pathways such as gluconeogenesis and TCA have inhibition potential against pathogenic bacteria (Hu et al., 2022). Enhanced biosynthesis of peptidoglycan may increase the abundance of lactic acid bacteria populations in the gut, partially facilitating the growth benefits. (Lee et al., 2022). Peptidoglycan can exert anti-inflammatory roles in the intestinal epithelia cells through the peptidoglycan recognition protein (Zenhom et al., 2012), indicating the anti-inflammatory roles of seaweed. Taken together, brown seaweed influences microbial functional metabolism, which may have an important role in changing the cecal microbiota composition in birds exposed to heat stress.

Heat stress can adversely affect gut morphology, evidenced by reduced villus height and increased crypt depth and reduced villus height to crypt depth ratio (Al-Fataftah and Abdelqader, 2014; Zhang et al., 2017; Song et al., 2018; Wu et al., 2018). In agreement with previous findings, our results showed that heat stress significantly reduced duodenal and ileal VH and VH: CD, and jejunal CD in broiler chickens, indicating a possible deterioration of intestinal health. This might lead to reduced feed intake in heat-stressed chickens, as shown in the first part of this study (Akinyemi and Adewole, 2022) and can adversely affect the growth of the birds. However, dietary supplementation of brown seaweed significantly increased the duodenal and ileal VH and VH:CD of heat-stressed birds which indicates that brown seaweed can protect against heat stress-impaired gut morphology. Our findings coincide with previous studies that reported improved intestinal morphology in chickens fed with seaweed polysaccharides (Guo et al., 2020; Liu et al., 2020). Meanwhile, heat stress challenge was not introduced in the aforementioned studies. The increase in VH and VH:CD among heat-stressed birds suggests that brown seaweed can increase the absorption of nutrients and improve nutrient digestibility and cell development (Wassie et al., 2021). The gut modulatory roles of brown seaweeds might be linked to their growth-promoting action that was previously observed in the first part of this study (Akinyemi and Adewole, 2022). Our results revalidated that brown seaweeds can serve as prebiotics that can enhance the growth and activity of beneficial microbes in the gastrointestinal tract. Prebiotics have various mechanisms of action, such as supplying nutrients to microorganisms, preventing pathogen attachment to host cells, modulating gut morphology, and affecting immune system functions (Pourabedin and Zhao, 2015). Brown seaweed may protect chickens from the negative impacts of stress and enhance their nutrient uptake in the gut. This could be due to the antioxidative and anti-inflammatory effects of brown seaweed (Begum et al., 2021).

In conclusion, dietary supplementation of brown seaweed enhanced beneficial bacteria, including Lactobacillus and improved intestinal morphology among heat-stressed birds. This indicates that seaweed could potentially be utilized as a dietary solution to alleviate heat stress-induced adverse effects on the gut health of broiler chickens.

ACKNOWLEDGMENTS

Our appreciation goes to Sealife Seaplants, NS, Canada, for supplying the seaweed products used in this study, and the staff of the Atlantic Poultry Research Centre – Michael McConkey, Sarah Macpherson, and Krista Budgell for help with animal care. Thanks to Janice MacIsaac for diet formulation and other logistics and Jamie Fraser for diet preparation. Appreciation goes to Taiwo Erinle, Taiwo Makinde, and Samson Oladokun for helping with feeding and sample collections. Funding for this study was provided by Nova Scotia Canadian Agricultural Partnership (CAP), Chicken Farmers of Nova Scotia, Canadian Poultry Research Council (CPRC), Mitacs, and NSERC discovery grant.

DISCLOSURES

The authors declare no conflict of interest.

Footnotes

1

Part of this work was presented at the 2023 PSA Annual Meeting, Philadelphia, United States.

Supplementary material associated with this article can be found in the online version at doi:10.1016/j.psj.2024.103562.

Appendix. Supplementary materials

mmc1.docx (20.8KB, docx)
mmc2.docx (265.6KB, docx)

REFERENCES

  1. Abdelqader A., Al-Fataftah A.R. Effect of dietary butyric acid on performance, intestinal morphology, microflora composition and intestinal recovery of heat-stressed broilers. Lives. Sci. 2016;183:78–83. [Google Scholar]
  2. Agregán R., Munekata P.E., Franco D., Carballo J., Barba F.J., Lorenzo J.M. Antioxidant potential of extracts obtained from macro-(Ascophyllum nodosum, Fucus vesiculosus and Bifurcaria bifurcata) and micro-algae (Chlorella vulgaris and Spirulina platensis) assisted by ultrasound. Medicines. 2018;5:33. doi: 10.3390/medicines5020033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ahmad R., Yu Y.H., Hsiao F.S.H., Su C.H., Liu H.C., Tobin I., Zhang G., Cheng Y.H. Influence of heat stress on poultry growth performance, intestinal inflammation, and immune function and potential mitigation by probiotics. Animals. 2022;12:2297. doi: 10.3390/ani12172297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Akinyemi F., Adewole D. Effects of brown seaweed products on growth performance, plasma biochemistry, immune response, and antioxidant capacity of broiler chickens challenged with heat stress. Poult. Sci. 2022;101 doi: 10.1016/j.psj.2022.102215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Al-Fataftah A.R., Abdelqader A. Effects of dietary Bacillus subtilis on heat-stressed broilers performance, intestinal morphology and microflora composition. Anim. Feed Sci. Technol. 2014;198:279–285. [Google Scholar]
  6. Arain M.A., Mei Z., Hassan F.U., Saeed M., Alagawany M., M., Shar A.H., Rajput I.R. Lycopene: a natural antioxidant for prevention of heat-induced oxidative stress in poultry. World's Poult. Sci. 2018;74:89–100. [Google Scholar]
  7. Archer G.S. Evaluation of an extract derived from the seaweed Ascophyllum nodosum to reduce the negative effects of heat stress on broiler growth and stress parameters. Animals. 2023;13:259. doi: 10.3390/ani13020259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Attia Y.A., Hassan R.A., Addeo N.F., Bovera F., Alhotan R.A., Al-Qurashi A.D., Al-Baadani H.H., Al-Banoby M.A., Khafaga A.F., Eisenreich W., Shehata A.A. Effects of spirulina platensis and/or allium sativum on antioxidant status, immune response, gut morphology, and intestinal lactobacilli and coliforms of heat-stressed broiler chicken. Vet. Sci. 2023;10:678. doi: 10.3390/vetsci10120678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ayo J.O., Ogbuagu N.E. Heat stress, haematology and small intestinal morphology in broiler chickens: insight into impact and antioxidant-induced amelioration. World's Poult. Sci. 2021;77:949–968. [Google Scholar]
  10. Bai H., Shi L., Guo Q., Jiang Y., Li X., Geng D., Chang G. Metagenomic insights into the relationship between gut microbiota and residual feed intake of small-sized meat ducks. Front. in Microbiol. 2023;13 doi: 10.3389/fmicb.2022.1075610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Balasubramanian B., Shanmugam S., Park S., Recharla N., Koo J.S., Andretta I., Kim I.H. Supplemental impact of marine red seaweed (Halymenia palmata) on the growth performance, total tract nutrient digestibility, blood profiles, intestine histomorphology, meat quality, fecal gas emission, and microbial counts in broilers. Animals: 2021;11:1244. doi: 10.3390/ani11051244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Begum R., Howlader S., Mamun-Or-Rashid A.N.M., Rafiquzzaman S.M., Ashraf G.M., Albadrani G.M., M G., Uddin M.S. Antioxidant and signal-modulating effects of brown seaweed-derived compounds against oxidative stress-associated pathology. Oxid. Med. Cell. Longev. 2021;2021 doi: 10.1155/2021/9974890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Borzouie S., Rathgeber B.M., Stupart C.M., MacIsaac J., MacLaren L.A. Effects of dietary inclusion of seaweed, heat stress and genetic strain on performance, plasma biochemical and hematological parameters in laying hens. Animals. 2020;10:1570. doi: 10.3390/ani10091570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Bettendorff L., Wins P. Thiamin diphosphate in biological chemistry: new aspects of thiamin metabolism, especially triphosphate derivatives acting other than as cofactors. FEBS. 2009;276:2917–2925. doi: 10.1111/j.1742-4658.2009.07019.x. [DOI] [PubMed] [Google Scholar]
  15. Bolyen E., Rideout J.R., Dillon M.R., Bokulich N.A., Abnet C.C., Al-Ghalith G.A., Caporaso J.G. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019;37:852–857. doi: 10.1038/s41587-019-0209-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Burgos S., Bohorquez D.V., Burgos S.A. Vitamin deficiency-induced neurological diseases of poultry. Int. J. Poult. Sci. 2006;5:804–807. [Google Scholar]
  17. Cavuoto P., Fenech M.F. A review of methionine dependency and the role of methionine restriction in cancer growth control and life-span extension. Cancer Treat. Rev. 2012;38:726–736. doi: 10.1016/j.ctrv.2012.01.004. [DOI] [PubMed] [Google Scholar]
  18. Charoensiddhi S., Conlon M.A., Methacanon P., Franco C.M.M., Su P., Zhang W. Gut health benefits of brown seaweed Ecklonia radiata and its polysaccharides demonstrated in vivo in a rat model. J. Funct. Foods. 2017;37:676–684. [Google Scholar]
  19. Charoensiddhi S., Conlon M., Methacanon P., Thayanukul P., Hongsprabhas P., Zhang W. Gut microbiome modulation and gastrointestinal digestibility in vitro of polysaccharide-enriched extracts and seaweeds from Ulva rigida and Gracilaria fisheri. J. Funct. Foods. 2022;96 [Google Scholar]
  20. Chaudhary A., Mishra P., Al Amaz S., Mahato P.L., Das R., Jha R., Mishra B. Dietary supplementation of microalgae mitigates the negative effects of heat stress in broilers. Poult. Sci. 2023;102 doi: 10.1016/j.psj.2023.102958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Coudert E., Baéza E., Berri C. Use of algae in poultry production: a review. World's Poult. Sci. 2020;76:767–786. [Google Scholar]
  22. Dash P.K., Hergenroeder G.W., Jeter C.B., Choi H.A., Kobori N., Moore A.N. Traumatic brain injury alters methionine metabolism: implications for pathophysiology. Front. Syst. Neurosci. 2016;10:36. doi: 10.3389/fnsys.2016.00036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Dierick N., Ovyn A., De Smet S. Effect of feeding intact brown seaweed Ascophyllum nodosum on some digestive parameters and on iodine content in edible tissues in pigs. J Sci Food Agric. 2009;89:584–594. [Google Scholar]
  24. Erinle T.J., Boulianne M., Adewole D. Red osier dogwood extract vs. trimethoprim-sulfadiazine (Part 2). Pharmacodynamic effects on ileal and cecal microbiota of broiler chickens challenged orally with Salmonella Enteritidis. Poult. Sci. 2023;102 doi: 10.1016/j.psj.2023.102550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Farkas V., Csitári G., Menyhárt L., Such N., Pál L., Husvéth F., Dublecz K. Microbiota composition of mucosa and interactions between the microbes of the different gut segments could be a factor to modulate the growth rate of broiler chickens. Animals. 2022;12:1296. doi: 10.3390/ani12101296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Feng P., Li Q., Sun H., Gao J., Ye X., Tao Y., Wang P. Effects of fulvic acid on growth performance, serum index, gut microbiota, and metabolites of Xianju yellow chicken. Front. in Nutr. 2022;9 doi: 10.3389/fnut.2022.963271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ferreira M., Teixeira C., Abreu H., Silva J., Costas B., Kiron V., Valente L.M. Nutritional value, antimicrobial and antioxidant activities of micro-and macroalgae, single or blended, unravel their potential use for aquafeeds. J. Appl. Phycol. 2021;33:3507–3518. [Google Scholar]
  28. Finegold S.M., Lawson. M. L. Vaisanen P.A., Molitoris D.R., Song Y., Liu C., Collins M.D. Anaerofustis stercorihominis gen. nov., sp. nov., from human feces. Anaerobe. 2004;10:41–45. doi: 10.1016/j.anaerobe.2003.10.002. [DOI] [PubMed] [Google Scholar]
  29. Goel A., Ncho C.M., Jeong C.M., V.Gupta J.Y.J., Ha S.Y., Yang J.K., Choi Y.H. Dietary supplementation of solubles from shredded, steam-exploded pine particles modifies gut length and cecum microbiota in cyclic heat-stressed broilers. Poult. Sci. 2023;102 doi: 10.1016/j.psj.2023.102498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Goel A., Ncho C.M., Jeong C.M., V.Gupta J.Y.J., Ha S.Y., Yang J.K. Effects of dietary supplementation of solubles from shredded, steam-exploded pine particles on the performance and cecum microbiota of acute heat-stressed broilers. Microorganisms. 2022;10:1795. doi: 10.3390/microorganisms10091795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gu F., Larsen N., Pascale N., Petersen S.A., Khakimov B., Respondek F., Jespersen L. Age-related effects on the modulation of gut microbiota by pectins and their derivatives: an in vitro study. Front. in Microbiol. 2023;14 doi: 10.3389/fmicb.2023.1207837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Guo Y., Zhao Z.H., Pan Z.Y., An L.L., Balasubramanian B., Liu W.C. New insights into the role of dietary marine-derived polysaccharides on productive performance, egg quality, antioxidant capacity, and jejunal morphology in late-phase laying hens. Poult Sci. 2020;99:2100–2107. doi: 10.1016/j.psj.2019.12.032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Gupta A., Chauhan N.R., Chowdhury D., Singh A., Meena R.C., Chakrabarti A., Singh S.B. Heat stress modulated gastrointestinal barrier dysfunction: role of tight junctions and heat shock proteins. Scand. J. Gastroenterol. 2017;52:1315–1319. doi: 10.1080/00365521.2017.1377285. [DOI] [PubMed] [Google Scholar]
  34. He X., Zhao S., Li Y. Faecalibacterium prausnitzii: a next-generation probiotic in gut disease improvement. Can. J. Infect. Dis. Med. Microbiol. 2021;10 Article ID 6666114. [Google Scholar]
  35. Holdt S.L., Kraan S. Bioactive compounds in seaweed: functional food applications and legislation. J. Appl. Phycol. 2011;23:543–597. [Google Scholar]
  36. Hu Y., Cai M., Chu W., Hu Y. Dysbiosis of gut microbiota and lipidomics of content induced by dietary methionine restriction in rice field eel (Monopterus albus) Front. Microbiol. 2022;13 doi: 10.3389/fmicb.2022.917051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Jahromi M.F., Liang J.B., Ebrahimi R., Soleimani A.F., Rezaeizadeh A., Abdullah N., Shokryazdan P. Protective potential of Lactobacillus species in lead toxicity model in broiler chickens. Animal. 2017;11:755–761. doi: 10.1017/S175173111600224X. [DOI] [PubMed] [Google Scholar]
  38. Jiao S., Zheng Z., Zhuang Y., Tang C., Zhang N. Dietary medium-chain fatty acid and Bacillus in combination alleviate weaning stress of piglets by regulating intestinal microbiota and barrier function. J. Anim. Sci. 2023;101:skac414. doi: 10.1093/jas/skac414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kamarudin A.N., Lai K.S., Lamasudin D.U., Idris A.S., Balia Yusof Z.N. Enhancement of thiamine biosynthesis in oil palm seedlings by colonization of endophytic fungus Hendersonia toruloidea. Front. in Plant Sci. 2017;8:1799. doi: 10.3389/fpls.2017.01799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kim J.Y., Kwon Y.M., Kim I.S., Kim J.A., Yu D.Y., Adhikari B., Cho K.K. Effects of the brown seaweed Laminaria japonica supplementation on serum concentrations of IgG, triglycerides, and cholesterol, and intestinal microbiota composition in rats. Front. in Nutr. 2018;5:23. doi: 10.3389/fnut.2018.00023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1. doi: 10.1093/nar/gks808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kogut M.H., Yin X., Yuan J., Broom L. Gut health in poultry. CAB Rev. 2017;12:1–7. [Google Scholar]
  43. Kong Q., Zhang R., You L., Ma Y., Liao L., Pedisić S. In vitro fermentation characteristics of polysaccharide from Sargassum fusiforme and its modulation effects on gut microbiota. Food Chem. Toxicol. 2021;151 doi: 10.1016/j.fct.2021.112145. [DOI] [PubMed] [Google Scholar]
  44. Kumari N.R.K., Nath D.N. Ameliorative measures to counter heat stress in poultry. World's Poult. Sci. J. 2018;74:117–130. [Google Scholar]
  45. Langille M.G., Zaneveld J., Caporaso J.G., McDonald D., Knights D., Reyes J.A., Huttenhower C. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. biotechnol. 2013;31:814–821. doi: 10.1038/nbt.2676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. La Reau A.J., Suen G. The Ruminococci: key symbionts of the gut ecosystem. J. Microbiol. 2018;56:199–208. doi: 10.1007/s12275-018-8024-4. [DOI] [PubMed] [Google Scholar]
  47. Lakshmanan A.P., Al Zaidan S., Bangarusamy D.K., Al-Shamari S., Elhag W., Terranegra A. Increased relative abundance of ruminoccocus is associated with reduced cardiovascular risk in an obese population. Front. Nutr. 2022;9 doi: 10.3389/fnut.2022.849005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Lee M., Park H., Heo J.M., Choi H.J., Seo S. Multi-tissue transcriptomic analysis reveals that L-methionine supplementation maintains the physiological homeostasis of broiler chickens than D-methionine under acute heat stress. Plos One. 2021;16 doi: 10.1371/journal.pone.0246063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Lee T.T., Chou C.H., Wang C., Lu H.Y., Yang W.Y. Bacillus amyloliquefaciens and Saccharomyces cerevisiae feed supplements improve growth performance and gut mucosal architecture with modulations on cecal microbiota in red-feathered native chickens. Anim. Biosci. 2022;35:869–883. doi: 10.5713/ab.21.0318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Liu W.C., Guo Y., Zhihui Z., Jha R., Balasubramanian B. Algae-derived polysaccharides promote growth performance by improving antioxidant capacity and intestinal barrier function in broiler chickens. Front Vet Sci. 2020;7:990. doi: 10.3389/fvets.2020.601336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Liu W.C., Zhu Y.R., Zhao Z.H., Jiang P., Yin F.Q. Effects of dietary supplementation of algae-derived polysaccharides on morphology, tight junctions, antioxidant capacity and immune response of duodenum in broilers under heat stress. Animals. 2021;11:2279. doi: 10.3390/ani11082279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Liu W.C., Zhuang D.P., Zhao Y., Balasubramanian B., Zhao Z.H. Seaweed-derived polysaccharides attenuate heat stress-induced splenic oxidative stress and inflammatory response via regulating Nrf2 and NF-κB signaling pathways. Marine Drugs. 2022;20:358. doi: 10.3390/md20060358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Liu W.C., Huang M.Y., Balasubramanian B., Jha R. Heat stress affects jejunal immunity of Yellow-feathered broilers and is potentially mediated by the microbiome. Front. Physiol. 2022;13:1022. doi: 10.3389/fphys.2022.913696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Liu Y., Feng Y., Yang X., Lv Z., Li P., Zhang M., Wei F., Jin X., Hu Y., Guo Y., Liu D. Mining chicken ileal microbiota for immunomodulatory microorganisms. ISME J. 2023;17:758–774. doi: 10.1038/s41396-023-01387-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Mohammadigheisar M., Shouldice V.L., Sands J.S., Lepp D., Diarra M.S., Kiarie E.G. Growth performance, breast yield, gastrointestinal ecology and plasma biochemical profile in broiler chickens fed multiple doses of a blend of red, brown and green seaweeds. Br. Poult. Sci. 2020;61:590–598. doi: 10.1080/00071668.2020.1774512. [DOI] [PubMed] [Google Scholar]
  56. Michalak I., Tiwari R., Dhawan M., Alagawany M., Farag M.R., Sharun K., Emran T.B., Dhama K. Antioxidant effects of seaweeds and their active compounds on animal health and production - a review. Vet. Quarterly. 2022;42:48–67. doi: 10.1080/01652176.2022.2061744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Mishra P., Das R., Chaudhary A., Mishra B., Jha R. Effects of microalgae, with or without xylanase supplementation, on growth performance, organs development, and gut health parameters of broiler chickens. Poult. Sci. 2023;102 doi: 10.1016/j.psj.2023.103056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Muñoz M., Guerrero-Araya E., Cortés-Tapia C., Plaza-Garrido A., Lawley T.D., Paredes-Sabja D. Comprehensive genome analyses of Sellimonas intestinalis, a potential biomarker of homeostasis gut recovery. Microb. Genom. 2020;6 doi: 10.1099/mgen.0.000476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Nanto-Hara F., Kikusato M., Ohwada S., Toyomizu M. Heat stress directly affects intestinal integrity in broiler chickens. J. Poult. Sci. 2020;57:284–290. doi: 10.2141/jpsa.0190004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Njoku E.N., Mottawea W., Hassan H., Hammami R. Prebiotic capacity of novel bioengineered wheat arabinoxylans in a batch culture model of the human gut microbiota. Front. in Microb. 2023;2 [Google Scholar]
  61. Ogita T., Yamamoto Y., Mikami A., Shigemori S., Sato T., Shimosato T. Oral administration of Flavonifractor plautii strongly suppresses Th2 immune responses in mice. Front. Immunol. 2020;11:379. doi: 10.3389/fimmu.2020.00379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Oladokun S., Clark K.F. Microbiota and transcriptomic effects of an essential oil blend and its delivery route compared to an antibiotic growth promoter in broiler chickens. Microorganisms. 2022;10:861. doi: 10.3390/microorganisms10050861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Oladokun S., MacIsaac J., Rathgeber B., Adewole D. Essential oil delivery route: effect on broiler chicken's growth performance, blood biochemistry, intestinal morphology, immune, and antioxidant status. Animals. 2021;11:3386. doi: 10.3390/ani11123386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Oladokun S., Adewole D. The effect of Bacillus subtilis and its delivery route on hatch and growth performance, blood biochemistry, immune status, gut morphology, and microbiota of broiler chickens. Poult. Sci. 2023;102 doi: 10.1016/j.psj.2022.102473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Patel A.K., Singhania R.R., Awasthi M.K., Varjani S., Bhatia S.K., Tsai M.L., Hsieh S.L., Chen C.W., Dong C.D. Emerging prospects of macro-and microalgae as prebiotic. Microbial Cell Factories. 2021;20:112. doi: 10.1186/s12934-021-01601-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Park J.K. Algal polysaccharides: properties and applications. Biochem. Anal. Biochem. 2015;4:1–2. [Google Scholar]
  67. Pourabedin M., Zhao X. Prebiotics and gut microbiota in chickens. FEMS Microbiol. Lett. 2015;362:1–8. doi: 10.1093/femsle/fnv122. [DOI] [PubMed] [Google Scholar]
  68. Quinteiro-Filho W.M., Gomes A.V.S., Pinheiro M.L., Ribeiro A., Ferraz-de-Paula V., Astolfi-Ferreira C.S., Ferreira A.J.P., Palermo-Neto J. Heat stress impairs performance and induces intestinal inflammation in broiler chickens infected with Salmonella Enteritidis. Avian Pathol. 2012;41:421–427. doi: 10.1080/03079457.2012.709315. [DOI] [PubMed] [Google Scholar]
  69. Quinteiro-Filho W.M., Ribeiro A., Ferraz-de-Paula V., Pinheiro M.L., Sakai M., Sá L.R., Ferreira M.A.J.P., Palermo-Neto J. Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poult. Sci. 2010;89:1905–1914. doi: 10.3382/ps.2010-00812. [DOI] [PubMed] [Google Scholar]
  70. Rinttilä T., Apajalahti J. Intestinal microbiota and metabolites-implications for broiler chicken health and performance. J. Appl. Poult. Res. 2013;22:647–658. [Google Scholar]
  71. Rostagno M.H. Effects of heat stress on the gut health of poultry. J. Anim. Sci. 2020;98:skaa090. doi: 10.1093/jas/skaa090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Shi D., Bai L., Qu Q., Zhou S., Yang M., Guo S., Li Q., Liu C. Impact of gut microbiota structure in heat-stressed broilers. Poult. Sci. 2019;98:2405–2413. doi: 10.3382/ps/pez026. [DOI] [PubMed] [Google Scholar]
  73. Shin J.H., Lee Y., Song E.J., Lee D., Jang S.Y., Byeon H.R., Nam Y.D. Faecalibacterium prausnitzii prevents hepatic damage in a mouse model of NASH induced by a high-fructose high-fat diet. Front. Microbiol. 2023;14 doi: 10.3389/fmicb.2023.1123547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Sokol H., Pigneur B., Watterlot L., O.Lakhdari L.G.B.-H., Gratadoux J.J., Langella P. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. 2008;105:16731–16736. doi: 10.1073/pnas.0804812105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Song Z.H., Cheng K., Zheng X.C., Ahmad H., Zhang L.L., Wang T. Effects of dietary supplementation with enzymatically treated Artemisia annua on growth performance, intestinal morphology, digestive enzyme activities, immunity, and antioxidant capacity of heat-stressed broilers. Poult. Sci. 2018;97:430–437. doi: 10.3382/ps/pex312. [DOI] [PubMed] [Google Scholar]
  76. Sumanu V.O., Naidoo V., Oosthuizen M.C. Adverse effects of heat stress during summer on broiler chickens production and antioxidant mitigating effects. Int. J. Biometeorol. 2022;66:2379–2393. doi: 10.1007/s00484-022-02372-5. [DOI] [PubMed] [Google Scholar]
  77. Sweeney T., Meredith H., Ryan M.T., Gath V., Thornton K., O'Doherty J.V. Effects of Ascophyllum nodosum supplementation on Campylobacter jejuni colonisation, performance and gut health following an experimental challenge in 10 day old chicks. Innov. Food Sci. Emerg. Technol. 2016;37:247–252. [Google Scholar]
  78. Takeshita N., Watanabe T., Ishida-Kuroki K. Transition of microbiota in chicken cecal droppings from commercial broiler farms. BMC Vet Res. 2021;17:10. doi: 10.1186/s12917-020-02688-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Van Dalen R., Peschel A., Van Sorge N.M. Wall teichoic acid in Staphylococcus aureus host interaction. Trends Microbiol. 2020;28:985–998. doi: 10.1016/j.tim.2020.05.017. [DOI] [PubMed] [Google Scholar]
  80. Vandana G.D., Sejian V., Lees A.M., Pragna P., Silpa M.V., Maloney S.K. Heat stress and poultry production: impact and amelioration. Int. J. Biometeorol. 2021;65:163–179. doi: 10.1007/s00484-020-02023-7. [DOI] [PubMed] [Google Scholar]
  81. Wang G., Li X., Zhou Y., Feng J., Zhang M. Effects of heat stress on gut-microbial metabolites, gastrointestinal peptides, glycolipid metabolism, and performance of broilers. Animals. 2021;11:1286. doi: 10.3390/ani11051286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Wang J., Cao H., Bao C., Liu Y., Dong B., Wang C., Liu S. Effects of xylanase in corn-or wheat-based diets on cecal microbiota of broilers. Front. Microbiol. 2021;12 doi: 10.3389/fmicb.2021.757066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Wang J., Lang T., Shen J., Dai J., Tian L., Wang X. Core gut bacteria analysis of healthy mice. Front. Microbiol. 2019;10:887. doi: 10.3389/fmicb.2019.00887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Wang W., Zhu J., Cao Q., Zhang C., Dong Z., Feng D., Zuo J. Dietary catalase supplementation alleviates deoxynivalenol-induced oxidative stress and gut microbiota dysbiosis in broiler chickens. Toxins. 2022;14:830. doi: 10.3390/toxins14120830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Wassie T., Lu Z., Duan X., Xie C., Gebeyew K., Yumei Z., Wu X. Dietary enteromorpha polysaccharide enhances intestinal immune response, integrity, and caecal microbial activity of broiler chickens. Front. Nutr. 2021;8 doi: 10.3389/fnut.2021.783819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Wu Q.J., Liu N., Wu X.H., Wang G.Y., Lin L. Glutamine alleviates heat stress-induced impairment of intestinal morphology, intestinal inflammatory response, and barrier integrity in broilers. Poult. Sci. 2018;97:2675–2683. doi: 10.3382/ps/pey123. [DOI] [PubMed] [Google Scholar]
  87. Xiang S., Ye K., Li M., Ying J., Wang H., Han J. Xylitol enhances synthesis of propionate in the colon via cross-feeding of gut microbiota. Microbiome. 2021;9:62. doi: 10.1186/s40168-021-01029-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Xu D., Feng M., Chu Y., Wang S., Shete V., Tuohy K.M., Yang Y. The prebiotic effects of oats on blood lipids, gut microbiota, and short-chain fatty acids in mildly hypercholesterolemic subjects compared with rice: a randomized, controlled trial. Front. Immunol. 2021;12 doi: 10.3389/fimmu.2021.787797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Zenhom M., Hyder A., De Vrese M., Heller K.J., Roeder T., Schrezenmeir J. Peptidoglycan recognition protein 3 (PglyRP3) has an anti-inflammatory role in intestinal epithelial cells. Immunobiology. 2012;217:412–419. doi: 10.1016/j.imbio.2011.10.013. [DOI] [PubMed] [Google Scholar]
  90. Zhang C., Zhao X.H., Yang L., Chen X.Y., Jiang R.S., Jin S.H., Geng Z.Y. Resveratrol alleviates heat stress-induced impairment of intestinal morphology, microflora, and barrier integrity in broilers. Poult. Sci. 2017;96:4325–4332. doi: 10.3382/ps/pex266. [DOI] [PubMed] [Google Scholar]
  91. Zhu Q., Song M., Azad M.A.K., Cheng Y., Liu Y., Liu Y., Kong X. Probiotics or synbiotics addition to sows’ diets alters colonic microbiome composition and metabolome profiles of offspring pigs. Front. Microbiol. 2022;13 doi: 10.3389/fmicb.2022.934890. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

mmc1.docx (20.8KB, docx)
mmc2.docx (265.6KB, docx)

Articles from Poultry Science are provided here courtesy of Elsevier

RESOURCES