Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis

Abstract Background Algivorous sea urchins can obtain energy from a diet of a single algal species, which may result in consequent changes in their gut microbe assemblies and association networks. Methods To ascertain whether such changes are led by specific microbes or limited to a specific region...

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Autores principales:	Matan Masasa, Ariel Kushmaro, Esti Kramarsky-Winter, Muki Shpigel, Roy Barkan, Alex Golberg, Abraham Kribus, Nadav Shashar, Lior Guttman
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Veterinary medicine SF600-1100 Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5a4d7363540c4eb7b490a24686fe40a7
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spelling	oai:doaj.org-article:5a4d7363540c4eb7b490a24686fe40a72021-11-21T12:29:00ZMono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis10.1186/s42523-021-00140-12524-4671https://doaj.org/article/5a4d7363540c4eb7b490a24686fe40a72021-11-01T00:00:00Zhttps://doi.org/10.1186/s42523-021-00140-1https://doaj.org/toc/2524-4671Abstract Background Algivorous sea urchins can obtain energy from a diet of a single algal species, which may result in consequent changes in their gut microbe assemblies and association networks. Methods To ascertain whether such changes are led by specific microbes or limited to a specific region in the gut, we compared the microbial assembly in the three major gut regions of the sea urchin Tripneustes gratilla elatensis when fed a mono-specific algal diet of either Ulva fasciata or Gracilaria conferta, or an algal-free diet. DNA extracts from 5 to 7 individuals from each diet treatment were used for Illumina MiSeq based 16S rRNA gene sequencing (V3–V4 region). Niche breadth of each microbe in the assembly was calculated for identification of core, generalist, specialist, or unique microbes. Network analyzers were used to measure the connectivity of the entire assembly and of each of the microbes within it and whether it altered with a given diet or gut region. Lastly, the predicted metabolic functions of key microbes in the gut were analyzed to evaluate their potential contribution to decomposition of dietary algal polysaccharides. Results Sea urchins fed with U. fasciata grew faster and their gut microbiome network was rich in bacterial associations (edges) and networking clusters. Bacteroidetes was the keystone microbe phylum in the gut, with core, generalist, and specialist representatives. A few microbes of this phylum were central hub nodes that maintained community connectivity, while others were driver microbes that led the rewiring of the assembly network based on diet type through changes in their associations and centrality. Niche breadth agreed with microbes' richness in genes for carbohydrate active enzymes and correlated Bacteroidetes specialists to decomposition of specific polysaccharides in the algal diets. Conclusions The dense and well-connected microbial network in the gut of Ulva-fed sea urchins, together with animal's rapid growth, may suggest that this alga was most nutritious among the experimental diets. Our findings expand the knowledge on the gut microbial assembly in T. gratilla elatensis and strengthen the correlation between microbes’ generalism or specialism in terms of occurrence in different niches and their metabolic arsenal which may aid host nutrition.Matan MasasaAriel KushmaroEsti Kramarsky-WinterMuki ShpigelRoy BarkanAlex GolbergAbraham KribusNadav ShasharLior GuttmanBMCarticleVeterinary medicineSF600-1100MicrobiologyQR1-502ENAnimal Microbiome, Vol 3, Iss 1, Pp 1-21 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Veterinary medicine SF600-1100 Microbiology QR1-502
spellingShingle	Veterinary medicine SF600-1100 Microbiology QR1-502 Matan Masasa Ariel Kushmaro Esti Kramarsky-Winter Muki Shpigel Roy Barkan Alex Golberg Abraham Kribus Nadav Shashar Lior Guttman Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis
description	Abstract Background Algivorous sea urchins can obtain energy from a diet of a single algal species, which may result in consequent changes in their gut microbe assemblies and association networks. Methods To ascertain whether such changes are led by specific microbes or limited to a specific region in the gut, we compared the microbial assembly in the three major gut regions of the sea urchin Tripneustes gratilla elatensis when fed a mono-specific algal diet of either Ulva fasciata or Gracilaria conferta, or an algal-free diet. DNA extracts from 5 to 7 individuals from each diet treatment were used for Illumina MiSeq based 16S rRNA gene sequencing (V3–V4 region). Niche breadth of each microbe in the assembly was calculated for identification of core, generalist, specialist, or unique microbes. Network analyzers were used to measure the connectivity of the entire assembly and of each of the microbes within it and whether it altered with a given diet or gut region. Lastly, the predicted metabolic functions of key microbes in the gut were analyzed to evaluate their potential contribution to decomposition of dietary algal polysaccharides. Results Sea urchins fed with U. fasciata grew faster and their gut microbiome network was rich in bacterial associations (edges) and networking clusters. Bacteroidetes was the keystone microbe phylum in the gut, with core, generalist, and specialist representatives. A few microbes of this phylum were central hub nodes that maintained community connectivity, while others were driver microbes that led the rewiring of the assembly network based on diet type through changes in their associations and centrality. Niche breadth agreed with microbes' richness in genes for carbohydrate active enzymes and correlated Bacteroidetes specialists to decomposition of specific polysaccharides in the algal diets. Conclusions The dense and well-connected microbial network in the gut of Ulva-fed sea urchins, together with animal's rapid growth, may suggest that this alga was most nutritious among the experimental diets. Our findings expand the knowledge on the gut microbial assembly in T. gratilla elatensis and strengthen the correlation between microbes’ generalism or specialism in terms of occurrence in different niches and their metabolic arsenal which may aid host nutrition.
format	article
author	Matan Masasa Ariel Kushmaro Esti Kramarsky-Winter Muki Shpigel Roy Barkan Alex Golberg Abraham Kribus Nadav Shashar Lior Guttman
author_facet	Matan Masasa Ariel Kushmaro Esti Kramarsky-Winter Muki Shpigel Roy Barkan Alex Golberg Abraham Kribus Nadav Shashar Lior Guttman
author_sort	Matan Masasa
title	Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis
title_short	Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis
title_full	Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis
title_fullStr	Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis
title_full_unstemmed	Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis
title_sort	mono-specific algal diets shape microbial networking in the gut of the sea urchin tripneustes gratilla elatensis
publisher	BMC
publishDate	2021
url	https://doaj.org/article/5a4d7363540c4eb7b490a24686fe40a7
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Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis

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