In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes

Karen Krüger,Meghan Chafee,Dörte Becher,Tijana Glavina Del Rio,T Ben Francis,Thomas Schweder,Hanno Teeling,Rudolf I Amann

doi:10.1038/s41396-019-0476-y

Abstract

We investigated Bacteroidetes during spring algae blooms in the southern North Sea in 2010–2012 using a time series of 38 deeply sequenced metagenomes. Initial partitioning yielded 6455 bins, from which we extracted 3101 metagenome-assembled genomes (MAGs) including 1286 Bacteroidetes MAGs covering ~120 mostly uncultivated species. We identified 13 dominant, recurrent Bacteroidetes clades carrying a restricted set of conserved polysaccharide utilization loci (PULs) that likely mediate the bulk of bacteroidetal algal polysaccharide degradation. The majority of PULs were predicted to target the diatom storage polysaccharide laminarin, alpha-glucans, alpha-mannose-rich substrates, and sulfated xylans. Metaproteomics at 14 selected points in time revealed expression of SusC-like proteins from PULs targeting all of these substrates. Analyses of abundant key players and their PUL repertoires over time furthermore suggested that fewer and simpler polysaccharides dominated early bloom stages, and that more complex polysaccharides became available as blooms progressed.

Highlights

Spring and summer blooms of planktonic microalgae are annually recurring phenomena in the world’s oceans’ temperate coastal regions
We obtained 1286 manually refined metagenome-assembled genomes (MAGs) affiliating with the Bacteroidetes phylum (Supplementary Table S2)
GTDB-Tk analysis [48] revealed that about 75% of the MAGs belonged to clades that we previously identified as key players during North Sea spring blooms of 2010–2012 [4, 5], including the Formosa (GTDB-Tk genus UBA3537), Polaribacter, Aurantivirga (GTDB-Tk genus SCGCAA160-P02), Candidatus Prosiliicoccus (GTDB-Tk genus HC6-5), the NS3a and NS5 marine groups (GTDB-Tk genera MAG-120531 and MS024-2A), and the GTDB-Tk genus-level clade MAG-121220-bin8, which all belong to the Flavobacteriaceae family (Fig. 1a, Supplementary Fig. S1)

Summary

Introduction

Spring and summer blooms of planktonic microalgae (phytoplankton) are annually recurring phenomena in the world’s oceans’ temperate coastal regions. A substantial portion of this organic matter consists of polysaccharides that act as algal storage compounds, cell wall components, and exudates. The proportion of these polysaccharides varies depending on algae species and growth stage, and ranges from 13% to ~90% of algal drymass [8].

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Results

Conclusion