Polysaccharide utilisation loci of Bacteroidetes from two contrasting open ocean sites in the North Atlantic

Abstract

Marine Bacteroidetes have pronounced capabilities of degrading high molecular weight organic matter such as proteins and polysaccharides. Previously we reported on 76 Bacteroidetes-affiliated fosmids from the North Atlantic Ocean's boreal polar and oligotrophic subtropical provinces. Here, we report on the analysis of further 174 fosmids from the same libraries. The combined, re-assembled dataset (226 contigs; 8.8 Mbp) suggests that planktonic Bacteroidetes at the oligotrophic southern station use more peptides and bacterial and animal polysaccharides, whereas Bacteroidetes at the polar station (East-Greenland Current) use more algal and plant polysaccharides. The latter agrees with higher abundances of algae and terrigenous organic matter, including plant material, at the polar station. Results were corroborated by in-depth bioinformatic analysis of 14 polysaccharide utilisation loci from both stations, suggesting laminarin-specificity for four and specificity for sulfated xylans for two loci. In addition, one locus from the polar station supported use of non-sulfated xylans and mannans, possibly of plant origin. While peptides likely represent a prime source of carbon for Bacteroidetes in open oceans, our data suggest that as yet unstudied clades of these Bacteroidetes have a surprisingly broad capacity for polysaccharide degradation. In particular, laminarin-specific PULs seem widespread and thus must be regarded as globally important.

Deterministic influences exceed dispersal effects on hydrologically‐connected microbiomes

“…Microbiomes with a diverse community of Proteobacteria may therefore be well‐adapted to fluctuations in organic C availability, facilitating their persistence across all zones. Moreover, Bacteriodetes has been shown to be prevalent in both waterborne and biofilm microbiomes in other systems – preferentially degrading recalcitrant C compounds and recycling biomass (Cottrell and Kirchman, ; Martin et al ., ; Bennke et al ., ). The presence of Bacteroidetes in addition to Proteobacteria within nearshore and river microbiomes may therefore indicate niche complementarity within these higher‐C environments, possibly coincident with spatial organization that is not captured in our measurements.…”

Polysaccharide Utilization Loci: Fueling Microbial Communities

“…1) through (meta)genomic, transcriptomic, and proteomic approaches (93)(94)(95)(96). PULs have been identified in species outside the Bacteroides genus in diverse environments, including the ruminal Prevotella bryantii (97), the freshwater dweller Flavobacterium johnsoniae (98), and the gut microbiota of the termite Pseudacanthotermes militaris (99).…”

Repeated evolutionary transitions of flavobacteria from marine to non‐marine habitats

“…The polysaccharide utilization locus (PUL) is an operon for binding, hydrolysis and uptake of polysaccharides (Bennke et al, 2016). A complete PUL contains genes encoding an outer membrane transporter SusC homologue known as TonB-dependent receptors (susC-type TBDR), and a co-located outer membrane substrate binding protein SusD, which is unique to Flavobacteriaceae and other lineages in the Bacteroidetes phylum (Anderson and Salyers, 1989;Thomas et al, 2011).…”

“…Within PULs, SusC and SusD homologues can be co-located with CAZymes and auxiliary genes such as sulfatase and regulatory factors. Polysaccharide utilization is often initiated by attaching them to SusD followed by extracellular or outer membrane enzymatic depolymerization of polysaccharides to oligosaccharides, the latter transported across the cell wall by TBDR for further utilization by CAZymes located at the periplasm, inner membrane and cytoplasm (Bennke et al, 2016). The absence of the associated SusD leads to an incomplete PUL and in this case, the SusC homologue is referred to as fhuA-type TBDR, which is specialized in uptake of oligosaccharides or small molecules (Ferguson et al, 1998).…”