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

Matan Masasa,Ariel Kushmaro,Abraham Kribus,Roy Barkan,Alex Golberg,Nadav Shashar,Lior Guttman,Muki Shpigel,Esti Kramarsky-Winter

doi:10.1186/s42523-021-00140-1

Abstract

BackgroundAlgivorous 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.MethodsTo 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.ResultsSea 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.ConclusionsThe 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.

Highlights

Algivorous sea urchins can obtain energy from a diet of a single algal species, which may result in con‐ sequent changes in their gut microbe assemblies and association networks
Diet shapes the gut microbe assembly of T. gratilla elatensis No mortality or morbidity of sea urchins was observed during the entire period of the feeding trial
The fifty-one samples that reached sequencing depth of 10,000 reads resulted in 988,513 high-quality reads (18,305 ± 5208 per sample) that were clustered into 434 unique Operational taxonomic unit (OTU) (117 ± 48 per sample; Additional file 1: Table S3)

Summary

Introduction

Algivorous sea urchins can obtain energy from a diet of a single algal species, which may result in con‐ sequent changes in their gut microbe assemblies and association networks. The ability of microbes to colonize different niches, i.e., their niche breadth, determines the composition and networking of the microbial assembly when challenged by various environmental forces [1]. With the constant development of new tools for analyzing microbial communities, specific platforms for network analyses have emerged. These tools allow the discrimination of association networks following their topologies as to density, clustering rate, diameter, length of shortest path, and other indices [4]. The connectivity of microbe nodes is not disrupted since many microbial nodes can be reached by any other node through a short number of steps, and the associating nodes are more likely to be neighbors of each other [6]. Driver microbes with the greatest contribution to the rewiring of a network under a certain weight (i.e., niche) can be identified by the changes in their associating members, type of association, and centrality [8]

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Conclusion