Age, gut location and diet impact the gut microbiome of a tropical herbivorous surgeonfish

Parata, Lara; Nielsen, Shaun; Xing, Xing; Thomas, Torsten; Egan, Suhelen; Vergés, Adriana

doi:10.1093/femsec/fiz179

Cited by 28 publications

(27 citation statements)

References 74 publications

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“…sydneyanus (Clements et al, 2007 ; Moran et al, 2005 ). We again sampled free‐living animals collected from their natural environment and analysed gut contents from specific regions of the alimentary tract since microbial communities are known to vary along the gut of vertebrates (Donaldson et al, 2016 ), including fish (Jones et al, 2018 ; Parata et al, 2020 ). Sample variation due to season, temperature, location and food source was minimized by collecting all fish on the same day from the same site at Great Barrier Island, Hauraki Gulf.…”

Section: Discussionmentioning

confidence: 99%

Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish

et al. 2022

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Many marine herbivorous fishes harbour diverse microbial communities in the hindgut that can play important roles in host health and nutrition. Kyphosus sydneyanus is a temperate marine herbivorous fish that feeds predominantly on brown seaweeds. We employed 16S rRNA gene amplicon sequencing and gas chromatography to characterize microbial communities and their metabolites in different hindgut regions of six K. sydneyanus. Measurements were confined to three distal sections of the intestine, labelled III, IV and V from anterior to posterior. A total of 625 operational taxonomic units from 20 phyla and 123 genera were obtained. Bacteroidota, Firmicutes and Proteobacteria were the major phyla in mean relative abundance, which varied along the gut. Firmicutes (76%) was the most dominant group in section III, whereas Bacteroidota (69.3%) dominated section V. Total short‐chain fatty acid (SCFA) concentration was highest in sections IV and V, confirming active fermentation in these two most distal sections. The abundance of Bacteroidota correlated with propionate concentration in section V, while Firmicutes positively correlated with formate in sections III and IV. Acetate levels were highest in sections IV and V, which correlated with abundance of Bacteroidota. Despite differences in gut microbial community composition, SCFA profiles were consistent between individual fish in the different hindgut regions of K. sydneyanus, although proportions of SCFAs differed among gut sections. These findings demonstrate functional compartmentalization of the hindgut microbial community, highlighting the need for regional sampling when interpreting overall microbiome function. These results support previous work suggesting that hindgut microbiota in marine herbivorous fish are important to nutrition in some host species by converting dietary carbohydrates into metabolically useful SCFAs.

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Section: Discussionmentioning

confidence: 99%

Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish

et al. 2022

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“…Jones et al 2018 observed highest alpha diversity in the hindgut in the rabbitfish Siganus fuscescens while Gajardo et al 2016 found similar trends in the taxonomically and geographically distinct Atlantic Salmon Salmo salar [ 31 , 75 ]. However, the opposite pattern has also been found, suggesting that alpha diversity trends through the gut may vary by other factors besides gut region [ 23 , 24 , 29 , 30 ].…”

Section: Discussionmentioning

confidence: 99%

Fine scale transitions of the microbiota and metabolome along the gastrointestinal tract of herbivorous fishes

et al. 2022

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Background Gut microorganisms aid in the digestion of food by providing exogenous metabolic pathways to break down organic compounds. An integration of longitudinal microbial and chemical data is necessary to illuminate how gut microorganisms supplement the energetic and nutritional requirements of animals. Although mammalian gut systems are well-studied in this capacity, the role of microbes in the breakdown and utilization of recalcitrant marine macroalgae in herbivorous fish is relatively understudied and an emerging priority for bioproduct extraction. Here we use a comprehensive survey of the marine herbivorous fish gut microbial ecosystem via parallel 16S rRNA gene amplicon profiling (microbiota) and untargeted tandem mass spectrometry (metabolomes) to demonstrate consistent transitions among 8 gut subsections across five fish of the genus of Kyphosus. Results Integration of microbial phylogenetic and chemical diversity data reveals that microbial communities and metabolomes covaried and differentiated continuously from stomach to hindgut, with the midgut containing multiple distinct and previously uncharacterized microenvironments and a distinct hindgut community dominated by obligate anaerobes. This differentiation was driven primarily by anaerobic gut endosymbionts of the classes Bacteroidia and Clostridia changing in concert with bile acids, small peptides, and phospholipids: bile acid deconjugation associated with early midgut microbiota, small peptide production associated with midgut microbiota, and phospholipid production associated with hindgut microbiota. Conclusions The combination of microbial and untargeted metabolomic data at high spatial resolution provides a new view of the diverse fish gut microenvironment and serves as a foundation to understand functional partitioning of microbial activities that contribute to the digestion of complex macroalgae in herbivorous marine fish.

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“…Fish gut microbiota is influenced by trophic level ( Liu et al, 2016 ), season ( Neuman et al, 2016 ; Dulski et al, 2020 ), host habitat ( Dehler et al, 2017 ; Dulski et al, 2020 ), and intestinal section ( Parata et al, 2020 ). For example, herbivorous, omnivorous, and carnivorous are the main trophic levels of fish and exhibit differences in gut microbiome composition ( Liu et al, 2016 ; Egerton et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Host Species Influence the Gut Microbiota of Endemic Cold-Water Fish in Upper Yangtze River

Peng

Zhang

et al. 2022

Front. Microbiol.

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The fish gut microbiome plays an important role in nutrition absorption and energy metabolism. Studying the gut microbes of cold-water fish is important to understand the dietary adaptation strategies in extreme environments. In this study, the gut samples of Schizothorax wangchiachii (SW, herbivorous), Schizothorax kozlovi (SK, omnivorous), and Percocypris pingi (PP, carnivorous) in the upper Yangtze River were collected, and we sequenced 16S rRNA amplicon to study the potential relationship between gut microbes and host species. The results showed that gut microbial composition and diversity were significantly different between the three cold-water fishes. These fishes had different key taxa in their gut microbes, including bacteria involved in the breakdown of food (e.g., Cetobacterium, Aeromonas, and Clostridium sensu stricto 10). The highest alpha diversity indices (e.g., Chao 1 index) were identified in the herbivore (SW), followed by the carnivore (PP), and the lowest in the omnivore (SK). Non-metric multidimensional scaling (NMDS) results revealed that the gut microbial community of these species was different between host species. The neutral community model (NCM) showed that the microbial community structure of SW was shaped by stochastic processes, and the highest species dispersal was found in SW, followed by PP, and the lowest in SK. The results of niche breadth agreed with these findings. Our results demonstrated that host species influenced the gut microbiome composition, diversity, and microbial community assembly processes of the three cold-water fishes. These findings implied that the variation of gut microbiome composition and function plays a key role in digesting and absorbing nutrients from different foods in cold-water fish.

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Age, gut location and diet impact the gut microbiome of a tropical herbivorous surgeonfish

Cited by 28 publications

References 74 publications

Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish

Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish

Fine scale transitions of the microbiota and metabolome along the gastrointestinal tract of herbivorous fishes

Host Species Influence the Gut Microbiota of Endemic Cold-Water Fish in Upper Yangtze River

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