Biogeographical and seasonal dynamics of the marine Roseobacter community and ecological links to DMSP-producing phytoplankton

James O’Brien,Tim Kahlke,Mark V Brown,Nachshon Siboni,Jodie Van De Kamp,Levente Bodrossy,Justin R Seymour,Katherina Petrou,Naomi M Levine,Anna R Bramucci,Lauren F Messer,Erin L Mcparland,Martin Ostrowski

doi:10.1038/s43705-022-00099-3

Abstract

Ecological interactions between marine bacteria and phytoplankton play a pivotal role in governing the ocean’s major biogeochemical cycles. Among these, members of the marine Roseobacter Group (MRG) can establish mutualistic relationships with phytoplankton that are, in part, maintained by exchanges of the organosulfur compound, dimethylsulfoniopropionate (DMSP). Yet most of what is known about these interactions has been derived from culture-based laboratory studies. To investigate temporal and spatial co-occurrence patterns between members of the MRG and DMSP-producing phytoplankton we analysed 16S and 18S rRNA gene amplicon sequence variants (ASVs) derived from 5 years of monthly samples from seven environmentally distinct Australian oceanographic time-series. The MRG and DMSP-producer communities often displayed contemporaneous seasonality, which was greater in subtropical and temperate environments compared to tropical environments. The relative abundance of both groups varied latitudinally, displaying a poleward increase, peaking (MRG at 33% of total bacteria, DMSP producers at 42% of eukaryotic phototrophs) during recurrent spring-summer phytoplankton blooms in the most temperate site (Maria Island, Tasmania). Network analysis identified 20,140 significant positive correlations between MRG ASVs and DMSP producers and revealed that MRGs exhibit significantly stronger correlations to high DMSP producers relative to other DMSP-degrading bacteria (Pelagibacter, SAR86 and Actinobacteria). By utilising the power of a continental network of oceanographic time-series, this study provides in situ confirmation of interactions found in laboratory studies and demonstrates that the ecological dynamics of an important group of marine bacteria are shaped by the production of an abundant and biogeochemically significant organosulfur compound.

Highlights

Roseobacters are a globally ubiquitous group of heterotrophic bacteria found in marine surface waters [1]
By utilising the power of a continental network of oceanographic time-series, this study provides in situ confirmation of interactions found in laboratory studies and demonstrates that the ecological dynamics of an important group of marine bacteria are shaped by the production of an abundant and biogeochemically significant organosulfur compound
A total of 3359 18S sequences were identified as likely DMSP-producing phytoplankton and 1053 18S sequences identified as Australian Microbiome Initiative (AMI) marine microbes database likely non-DMSP producers (NoDP) (Supplementary Table S5)

Summary

Introduction

Roseobacters are a globally ubiquitous group of heterotrophic bacteria found in marine surface waters [1]. There are two primary degradation pathways for DMSP [23]: the DMSP lyase pathway, which cleaves DMSP to produce acrylate and the volatile gas, dimethylsulphide (DMS); and the DMSP demethylation pathway, which precludes DMS as a biproduct and results in the assimilation of DMSP-derived sulfur. The balance between these two pathways, which is Received: 3 August 2021 Revised: 26 January 2022 Accepted: 28 January 2022

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