North Sea spring bloom-associated Gammaproteobacteria fill diverse heterotrophic niches

Ben Francis,Hanno Teeling,Tim Urich,Annett Mikolasch,Rudolf Amann

doi:10.1186/s40793-021-00385-y

Abstract

BackgroundThe planktonic bacterial community associated with spring phytoplankton blooms in the North Sea is responsible for a large amount of carbon turnover in an environment characterised by high primary productivity. Individual clades belonging to the Gammaproteobacteria have shown similar population dynamics to Bacteroidetes species, and are thus assumed to fill competing ecological niches. Previous studies have generated large numbers of metagenome assembled genomes and metaproteomes from these environments, which can be readily mined to identify populations performing potentially important ecosystem functions. In this study we attempt to catalogue these spring bloom-associated Gammaproteobacteria, which have thus far attracted less attention than sympatric Alphaproteobacteria and Bacteroidetes.MethodsWe annotated 120 non-redundant species-representative gammaproteobacterial metagenome assembled genomes from spring bloom sampling campaigns covering the four years 2010–2012 and 2016 using a combination of Prokka and PfamScan, with further confirmation via BLAST against NCBI-NR. We also matched these gene annotations to 20 previously published metaproteomes covering those sampling periods plus the spring of 2009.ResultsMetagenome assembled genomes with clear capacity for polysaccharide degradation via dedicated clusters of carbohydrate active enzymes were among the most abundant during blooms. Many genomes lacked gene clusters with clearly identifiable predicted polysaccharide substrates, although abundantly expressed loci for the uptake of large molecules were identified in metaproteomes. While the larger biopolymers, which are the most abundant sources of reduced carbon following algal blooms, are likely the main energy source, some gammaproteobacterial clades were clearly specialised for smaller organic compounds. Their substrates range from amino acids, monosaccharides, and DMSP, to the less expected, such as terpenoids, and aromatics and biphenyls, as well as many ‘unknowns’. In particular we uncover a much greater breadth of apparent methylotrophic capability than heretofore identified, present in several order level clades without cultivated representatives.ConclusionsLarge numbers of metagenome assembled genomes are today publicly available, containing a wealth of readily accessible information. Here we identified a variety of predicted metabolisms of interest, which include diverse potential heterotrophic niches of spring bloom-associated Gammaproteobacteria. Features such as those identified here could well be fertile ground for future experimental studies.

Highlights

The planktonic bacterial community associated with spring phytoplankton blooms in the North Sea is responsible for a large amount of carbon turnover in an environment characterised by high primary productivity
It is clear that the bulk of the diversity in the samples we analysed—i.e. covering a small part of the pre-bloom period, and the main part of the spring blooms themselves in the four years 2010–2012 & 2016— was made up of species that reach higher relative abundances over time in response to the growth of algae
We have clearly identified a wider range of potential lifestyles, including growth on small organic molecules such as methanol and hydrocarbons, putative autotrophic and photoheterotrophic growth, and specialisation on amino acids, oligopeptides, sugar monomers, and oligosaccharides, in the Gammaproteobacteria

Summary

Introduction

The planktonic bacterial community associated with spring phytoplankton blooms in the North Sea is responsible for a large amount of carbon turnover in an environment characterised by high primary productivity. In this study we attempt to catalogue these spring bloom-associated Gammaproteobacteria, which have far attracted less attention than sympatric Alphaproteobacteria and Bacteroidetes. Three major clades of heterotrophic bacteria, namely the Alpha- and Gammaproteobacteria and the Bacteroidetes, have been found in many studies to grow in response to marine phytoplankton blooms [5,6,7,8,9,10]. While the Alpha- and Gammaproteobacteria and Bacteroidetes each account for similar proportions of the overall bacterial community during blooms in terms of inferred cell numbers, it is the Alphaproteobacteria and Bacteroidetes that have attracted greater attention to date We turn our attention to the Gammaproteobacteria, which are a significant part of both pre-bloom and bloom communities, and have been found to directly respond to the phytoplankton growth and decline in a similar fashion to the Bacteroidetes [7,8,9]

Methods

Results

Conclusion