Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts

Matthew J Neave,Craig T Michell,Christian R Voolstra,Amy Apprill

doi:10.1038/srep40579

Abstract

Endozoicomonas bacteria are globally distributed and often abundantly associated with diverse marine hosts including reef-building corals, yet their function remains unknown. In this study we generated novel Endozoicomonas genomes from single cells and metagenomes obtained directly from the corals Stylophora pistillata, Pocillopora verrucosa, and Acropora humilis. We then compared these culture-independent genomes to existing genomes of bacterial isolates acquired from a sponge, sea slug, and coral to examine the functional landscape of this enigmatic genus. Sequencing and analysis of single cells and metagenomes resulted in four novel genomes with 60–76% and 81–90% genome completeness, respectively. These data also confirmed that Endozoicomonas genomes are large and are not streamlined for an obligate endosymbiotic lifestyle, implying that they have free-living stages. All genomes show an enrichment of genes associated with carbon sugar transport and utilization and protein secretion, potentially indicating that Endozoicomonas contribute to the cycling of carbohydrates and the provision of proteins to their respective hosts. Importantly, besides these commonalities, the genomes showed evidence for differential functional specificity and diversification, including genes for the production of amino acids. Given this metabolic diversity of Endozoicomonas we propose that different genotypes play disparate roles and have diversified in concert with their hosts.

Highlights

Oceanospirillales; see Neave et al for review[14])
The sequencing and availability of these Endozoicomonas genomes from a diverse range of hosts, environments, and ecologies provides a solid foundation for understanding the functional diversity of Endozoicomonas, and our analysis provides new insight about their genomic similarities and functional characteristics
Endozoicomonas bacteria frequently associate with a diverse variety of marine hosts in oceans worldwide

Summary

Introduction

Oceanospirillales; see Neave et al for review[14]) These bacteria associate with a wide variety of marine hosts, including corals[15,16,17,18,19], and other cnidarians[20,21], sponges[22,23], gorgonians[24,25,26], molluscs[27,28], worms[29], fish[30,31], and tunicates[32,33]. A novel species of Endozoicomonas was responsible for epitheliocystis in the sharpsnout bream, Diplodus puntazzo[30] These opposing functions suggest that Endozoicomonas have multiple roles in their many hosts, and members from this genus may opportunistically transition through different symbiotic relationships, i.e., mutualistic, commensalistic, and parasitic. This is the first study to comparatively analyse Endozoicomonas genomes and provides important functional insight into this enigmatic genus

Methods

Results

Discussion

Conclusion