Abstract

Intestinal bacterial communities are highly relevant to the digestion, nutrition, growth, reproduction, and immunity of animals, but little is known about the composition and function of intestinal microbiota in deep-sea invertebrates. In this study, the intestinal microbiota of six holothurian Molpadia musculus were investigated, showing that their midguts were predominantly occupied by Izemoplasmatales bacteria. Using metagenomic sequencing, a draft genome of 1,822,181 bp was successfully recovered. After comparison with phylogenetically related bacteria, genes involved in saccharide usage and de novo nucleotide biosynthesis were reduced. However, a set of genes responsible for extracellular nucleoside utilization and 14 of 20 amino acid synthesis pathways were completely retained. Under oligotrophic condition, the gut-associated bacterium may make use of extracellular DNA for carbon and energy supplement, and may provide essential amino acids to the host. The clustered regularly interspaced short palindromic repeat (CRISPR) and restriction–modification (RM) systems presented in the genome may provide protection against invading viruses. A linear azol(in)e-containing peptide gene cluster for bacteriocin synthesize was also identified, which may inhibit the colonization and growth of harmful bacteria. Known virulence factors were not found by database searching. On the basis of its phylogenetic position and metabolic characteristics, we proposed that the bacterium represented a novel genus and a novel family within the Izemoplasmatales order and suggested it be named “Candidatus Bathyoplasma sp. NZ”. This was the first time describing host-associated Izemoplasmatales.

Highlights

  • Holothurians (Echinodermata: Holothuroidea) are marine invertebrates, presenting a wide vertical distribution from the intertidal zone to the deepest hadal trench

  • Proteobacteria and Epsilonbacteraeota accounted for the vast majority of microorganisms in the foreguts and hindguts of M. musculus

  • Some linear azol(in)e-containing peptides acted as toxins, such as listeriolysin S and streptolysin O, the predicted precursor peptide in this study showed no similarity with validated toxins

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Summary

Introduction

Holothurians (Echinodermata: Holothuroidea) are marine invertebrates, presenting a wide vertical distribution from the intertidal zone to the deepest hadal trench They dominate benthic megafaunal communities both in terms of quantity and biomass [1]. Organic debris is continuously decomposed and reused by various consumers during vertical landing and horizontal migration, and active organic matter such as proteinogenic amino acids, carbohydrates, and fatty acids are preferentially degraded, absorbed, and utilized [7]. This leads to refractory macromolecular materials (such as algaenan, cutin, suberin, and lignin that are derived from algae or higher plants) enriched in deep-sea sediments [3]

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