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

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.

Short‐term changes in polysaccharide utilization mechanisms of marine bacterioplankton during a spring phytoplankton bloom

“…These successional patterns are likely the result of finely tuned bacterial responses to changing organic matter availability derived from the phytoplankton. Specialist heterotrophic bacterial groups vary in their genomic repertoire (Bauer et al ., ; Xing et al ., ; Badur et al ., ; Unfried et al ., ; Kappelmann et al ., ; Krüger et al ., ), and thus in their ability to access complex substrates produced in abundance by phytoplankton; the progression during a bloom of autotrophic and heterotrophic members of the plankton is therefore closely intertwined (Buchan et al ., ). Measuring two distinct mechanisms of substrate processing while tracking dynamic changes in microbial community composition provides new insight into the conditions under which different strategies of substrate processing prevail.…”

“…A). These responses are likely due to increased quantity as well as higher complexity of organic matter available during the course of the bloom (Krüger et al ., ). Hel_1 was taken early in the first diatom bloom after the winter, conditions under which little bioavailable HMW organic matter would be present.…”

“…). These developing responses to the presence of specific polysaccharides likely reflected transitions in the bloom‐associated microbial community, with bacteria possessing the highly specific enzymes required to depolymerize more complex substrates increasingly present as the bloom progressed (Teeling et al ., ; Krüger et al ., ). Thus, in order to observe hydrolysis of specific complex substrates in our incubations, a starting community for a given incubation had to contain sufficient member(s) with the capability of responding to that complex substrate.…”

“…Within these taxa, successive bacterial groups grow and replace one another (Teeling et al ., ), with a marked temporal succession in key genes and proteins produced by individual bacterial groups that are linked with the processing of complex organic matter (Teeling et al ., , ). The nature and structures of the phytoplankton‐derived substrates targeted by specific bacterial groups is only beginning to be revealed through focused genetic and (meta‐)genomic analyses that indicate the substrate specialization of specific organisms (Teeling et al ., , ; Kappelmann et al ., ; Krüger et al ., ).…”

Short-term changes in polysaccharide utilization mechanisms of marine bacterioplankton during a spring phytoplankton bloom

“…2a). These responses are likely due to 337 increased quantity as well as higher complexity of organic matter available during the course of the 338 bloom (Krüger et al, 2019). Hel_1 was taken early in the first diatom bloom after the winter, 339 conditions under which little bioavailable HMW organic matter would be present.…”