Polysaccharide utilization loci of North Sea Flavobacteriia as basis for using SusC/D-protein expression for predicting major phytoplankton glycans

Lennart Kappelmann,Rudolf I Amann,Thomas Schweder,Stephanie Markert,Hanno Teeling,Nicole Shapiro,Frank Unfried,Jan-Hendrik Hehemann,Karen Krüger,Dörte Becher,Jens Harder

doi:10.1038/s41396-018-0242-6

Abstract

Marine algae convert a substantial fraction of fixed carbon dioxide into various polysaccharides. Flavobacteriia that are specialized on algal polysaccharide degradation feature genomic clusters termed polysaccharide utilization loci (PULs). As knowledge on extant PUL diversity is sparse, we sequenced the genomes of 53 North Sea Flavobacteriia and obtained 400 PULs. Bioinformatic PUL annotations suggest usage of a large array of polysaccharides, including laminarin, α-glucans, and alginate as well as mannose-, fucose-, and xylose-rich substrates. Many of the PULs exhibit new genetic architectures and suggest substrates rarely described for marine environments. The isolates’ PUL repertoires often differed considerably within genera, corroborating ecological niche-associated glycan partitioning. Polysaccharide uptake in Flavobacteriia is mediated by SusCD-like transporter complexes. Respective protein trees revealed clustering according to polysaccharide specificities predicted by PUL annotations. Using the trees, we analyzed expression of SusC/D homologs in multiyear phytoplankton bloom-associated metaproteomes and found indications for profound changes in microbial utilization of laminarin, α-glucans, β-mannan, and sulfated xylan. We hence suggest the suitability of SusC/D-like transporter protein expression within heterotrophic bacteria as a proxy for the temporal utilization of discrete polysaccharides.

Highlights

Half of global net primary production is oceanic and carried out mostly by small, unicellular phytoplankton such as diatoms [1]
Glenwright et al [7] showed that these two proteins form a ‘pedal bin’ complex in Bacteroides thetaiotaomicron, with SusD acting as a lid on top of the SusD-like protein sequences of the isolates’ PULs (SusC)-like TonB-dependent transporters (TBDTs)
The 53 flavobacterial isolates cover a broad range of the Flavobacteriia class within the phylogenetic tree based on full-length 16S rRNA genes (Fig. 1)

Summary

Introduction

Half of global net primary production is oceanic and carried out mostly by small, unicellular phytoplankton such as diatoms [1]. Polysaccharides account for up to 50% of algal biomass [2] and can be found as intracellular energy storage compounds, as structural components of their cell walls [3], or as secreted extracellular transparent exopolymeric substances [4]. Upon binding of a ligand, the SusD lid closes and conformational changes lead to substrate

Methods

Results

Conclusion