Metagenomic insights into zooplankton-associated bacterial communities.

Daniele De Corte,Marja Koski,Eva Sintes,Abhishek Srivastava,Yoshihiro Takaki,Juan Antonio L Garcia,Taichi Yokokawa,Gerhard J Herndl,Nathalie H Elisabeth,Takuro Nunoura

doi:10.1111/1462-2920.13944

Abstract

SummaryZooplankton and microbes play a key role in the ocean's biological cycles by releasing and consuming copious amounts of particulate and dissolved organic matter. Additionally, zooplankton provide a complex microhabitat rich in organic and inorganic nutrients in which bacteria thrive. In this study, we assessed the phylogenetic composition and metabolic potential of microbial communities associated with crustacean zooplankton species collected in the North Atlantic. Using Illumina sequencing of the 16S rRNA gene, we found significant differences between the microbial communities associated with zooplankton and those inhabiting the surrounding seawater. Metagenomic analysis of the zooplankton‐associated microbial community revealed a highly specialized bacterial community able to exploit zooplankton as microhabitat and thus, mediating biogeochemical processes generally underrepresented in the open ocean. The zooplankton‐associated bacterial community is able to colonize the zooplankton's internal and external surfaces using a large set of adhesion mechanisms and to metabolize complex organic compounds released or exuded by the zooplankton such as chitin, taurine and other complex molecules. Moreover, the high number of genes involved in iron and phosphorus metabolisms in the zooplankton‐associated microbiome suggests that this zooplankton‐associated bacterial community mediates specific biogeochemical processes (through the proliferation of specific taxa) that are generally underrepresented in the ambient waters.

Highlights

Zooplankton and microbes are fundamental components of the ocean’s lower food web
The high number of genes involved in iron and phosphorus metabolisms in the zooplankton-associated microbiome suggests that this zooplankton-associated bacterial community mediates specific biogeochemical processes that are generally underrepresented in the ambient waters
No significant differences were found between diversity, richness and evenness indexes of ambient water bacterial communities collected at different depth layers or between zooplankton–associated communities collected during the day versus night (ANOVA on rank, P>0.001) (Figs. 1 and S1, Table S1)

Summary

Introduction

Zooplankton and microbes are fundamental components of the ocean’s lower food web. Crustacean zooplankton release copious amounts of particulate organic matter (POM) originating from phytoplankton, heterotrophic microzooplankton and detritus into the ambient water (Heinle et al, 1977; Calbet, 2001). Heterotrophic microbes are responsible for most of the dissolved organic matter (DOM) mineralization in the open ocean (Azam et al, 1983; Cherrier et al, 1996) These two components of the marine food web are generally treated as separate entities only connected through the trophic cascades, albeit, microbes and zooplankton are dynamically linked at different ecological levels (Azam and Malfatti, 2007; Tang et al, 2010). The zooplankton’s acidic digestive tract may promote iron recycling and solubilization via multiple pathways involving microbes (Tang et al, 2011; Nuester et al, 2014; Schmidt et al, 2016) These processes deliver bioavailable iron to the ambient water that can be utilized by phytoplankton, promoting iron fertilization (Schmidt et al, 2016)

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