Cesar T Facimoto, Kendall D Clements, W Lindsey White, Kim M Handley
{"title":"类杆菌和梭状芽孢杆菌能够降解草食性鱼类 Kyphosus sydneyanus 后肠中的一系列多糖。","authors":"Cesar T Facimoto, Kendall D Clements, W Lindsey White, Kim M Handley","doi":"10.1093/ismeco/ycae102","DOIUrl":null,"url":null,"abstract":"<p><p>The gut microbiota of the marine herbivorous fish <i>Kyphosus sydneyanus</i> are thought to play an important role in host nutrition by supplying short-chain fatty acids (SCFAs) through fermentation of dietary red and brown macroalgae. Here, using 645 metagenome-assembled genomes (MAGs) from wild fish, we determined the capacity of different bacterial taxa to degrade seaweed carbohydrates along the gut. Most bacteria (99%) were unclassified at the species level. Gut communities and CAZyme-related transcriptional activity were dominated by <i>Bacteroidia</i> and <i>Clostridia</i>. Both classes possess genes CAZymes acting on internal polysaccharide bonds, suggesting their role initiating glycan depolymerization, followed by rarer <i>Gammaproteobacteria</i> and <i>Verrucomicrobiae</i>. Results indicate that <i>Bacteroidia</i> utilize substrates in both brown and red algae, whereas other taxa, namely, <i>Clostridia</i>, <i>Bacilli</i>, and <i>Verrucomicrobiae</i>, utilize mainly brown algae. <i>Bacteroidia</i> had the highest CAZyme gene densities overall, and <i>Alistipes</i> were especially enriched in CAZyme gene clusters (<i>n</i> = 73 versus just 62 distributed across all other taxa), pointing to an enhanced capacity for macroalgal polysaccharide utilization (e.g., alginate, laminarin, and sulfated polysaccharides). Pairwise correlations of MAG relative abundances and encoded CAZyme compositions provide evidence of potential inter-species collaborations. Co-abundant MAGs exhibited complementary degradative capacities for specific substrates, and flexibility in their capacity to source carbon (e.g., glucose- or galactose-rich glycans), possibly facilitating coexistence via niche partitioning. Results indicate the potential for collaborative microbial carbohydrate metabolism in the <i>K. sydneyanus</i> gut, that a greater variety of taxa contribute to the breakdown of brown versus red dietary algae, and that <i>Bacteroidia</i> encompass specialized macroalgae degraders.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae102"},"PeriodicalIF":5.1000,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11333855/pdf/","citationCount":"0","resultStr":"{\"title\":\"<i>Bacteroidia</i> and <i>Clostridia</i> are equipped to degrade a cascade of polysaccharides along the hindgut of the herbivorous fish <i>Kyphosus sydneyanus</i>.\",\"authors\":\"Cesar T Facimoto, Kendall D Clements, W Lindsey White, Kim M Handley\",\"doi\":\"10.1093/ismeco/ycae102\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The gut microbiota of the marine herbivorous fish <i>Kyphosus sydneyanus</i> are thought to play an important role in host nutrition by supplying short-chain fatty acids (SCFAs) through fermentation of dietary red and brown macroalgae. Here, using 645 metagenome-assembled genomes (MAGs) from wild fish, we determined the capacity of different bacterial taxa to degrade seaweed carbohydrates along the gut. Most bacteria (99%) were unclassified at the species level. Gut communities and CAZyme-related transcriptional activity were dominated by <i>Bacteroidia</i> and <i>Clostridia</i>. Both classes possess genes CAZymes acting on internal polysaccharide bonds, suggesting their role initiating glycan depolymerization, followed by rarer <i>Gammaproteobacteria</i> and <i>Verrucomicrobiae</i>. Results indicate that <i>Bacteroidia</i> utilize substrates in both brown and red algae, whereas other taxa, namely, <i>Clostridia</i>, <i>Bacilli</i>, and <i>Verrucomicrobiae</i>, utilize mainly brown algae. <i>Bacteroidia</i> had the highest CAZyme gene densities overall, and <i>Alistipes</i> were especially enriched in CAZyme gene clusters (<i>n</i> = 73 versus just 62 distributed across all other taxa), pointing to an enhanced capacity for macroalgal polysaccharide utilization (e.g., alginate, laminarin, and sulfated polysaccharides). Pairwise correlations of MAG relative abundances and encoded CAZyme compositions provide evidence of potential inter-species collaborations. Co-abundant MAGs exhibited complementary degradative capacities for specific substrates, and flexibility in their capacity to source carbon (e.g., glucose- or galactose-rich glycans), possibly facilitating coexistence via niche partitioning. Results indicate the potential for collaborative microbial carbohydrate metabolism in the <i>K. sydneyanus</i> gut, that a greater variety of taxa contribute to the breakdown of brown versus red dietary algae, and that <i>Bacteroidia</i> encompass specialized macroalgae degraders.</p>\",\"PeriodicalId\":73516,\"journal\":{\"name\":\"ISME communications\",\"volume\":\"4 1\",\"pages\":\"ycae102\"},\"PeriodicalIF\":5.1000,\"publicationDate\":\"2024-08-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11333855/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"ISME communications\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1093/ismeco/ycae102\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/1/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q1\",\"JCRName\":\"ECOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"ISME communications","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/ismeco/ycae102","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"ECOLOGY","Score":null,"Total":0}
Bacteroidia and Clostridia are equipped to degrade a cascade of polysaccharides along the hindgut of the herbivorous fish Kyphosus sydneyanus.
The gut microbiota of the marine herbivorous fish Kyphosus sydneyanus are thought to play an important role in host nutrition by supplying short-chain fatty acids (SCFAs) through fermentation of dietary red and brown macroalgae. Here, using 645 metagenome-assembled genomes (MAGs) from wild fish, we determined the capacity of different bacterial taxa to degrade seaweed carbohydrates along the gut. Most bacteria (99%) were unclassified at the species level. Gut communities and CAZyme-related transcriptional activity were dominated by Bacteroidia and Clostridia. Both classes possess genes CAZymes acting on internal polysaccharide bonds, suggesting their role initiating glycan depolymerization, followed by rarer Gammaproteobacteria and Verrucomicrobiae. Results indicate that Bacteroidia utilize substrates in both brown and red algae, whereas other taxa, namely, Clostridia, Bacilli, and Verrucomicrobiae, utilize mainly brown algae. Bacteroidia had the highest CAZyme gene densities overall, and Alistipes were especially enriched in CAZyme gene clusters (n = 73 versus just 62 distributed across all other taxa), pointing to an enhanced capacity for macroalgal polysaccharide utilization (e.g., alginate, laminarin, and sulfated polysaccharides). Pairwise correlations of MAG relative abundances and encoded CAZyme compositions provide evidence of potential inter-species collaborations. Co-abundant MAGs exhibited complementary degradative capacities for specific substrates, and flexibility in their capacity to source carbon (e.g., glucose- or galactose-rich glycans), possibly facilitating coexistence via niche partitioning. Results indicate the potential for collaborative microbial carbohydrate metabolism in the K. sydneyanus gut, that a greater variety of taxa contribute to the breakdown of brown versus red dietary algae, and that Bacteroidia encompass specialized macroalgae degraders.