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

Abstract

SummarySpring phytoplankton blooms in temperate environments contribute disproportionately to global marine productivity. Bloom-derived organic matter, much of it occurring as polysaccharides, fuels biogeochemical cycles driven by interacting autotrophic and heterotrophic communities. We tracked changes in the mode of polysaccharide utilization by heterotrophic bacteria during the course of a diatom-dominated bloom in the German Bight, North Sea. Polysaccharides can be taken up in a ‘selfish’ mode, where initial hydrolysis is coupled to transport into the periplasm, such that little to no low molecular weight (LMW) products are externally released to the environment. Alternatively, polysaccharides hydrolyzed by cell-surface attached or free extracellular enzymes (external hydrolysis) yield LMW products available to the wider bacterioplankton community. In the early bloom phase, selfish activity was accompanied by low extracellular hydrolysis rates of a few polysaccharides. As the bloom progressed, selfish uptake increased markedly, and external hydrolysis rates increased, but only for a limited range of substrates. The late bloom phase was characterized by high external hydrolysis rates of a broad range of polysaccharides, and reduced selfish uptake of polysaccharides, except for laminarin. Substrate utilization mode is related both to substrate structural complexity and to the bloom-stage dependent composition of the heterotrophic bacterial community.Originality statementThe means by which heterotrophic bacteria cooperate and compete to obtain substrates is a key factor determining the rate and location at which organic matter is cycled in the ocean. Much of this organic matter is high molecular weight (HMW), and must be enzymatically hydrolyzed to smaller pieces to be processed by bacterial communities. Some of these enzyme-producing bacteria are ‘selfish’, processing HMW organic matter without releasing low molecular weight (LMW) products to the environment. Other bacteria hydrolyze HMW substrates in a manner that releases LMW products to the wider bacterial community. How these mechanisms of substrate hydrolysis work against a changing background of organic matter supply is unclear. Here, we measured changing rates and mechanisms of substrate processing during the course of a natural phytoplankton bloom in the North Sea. Selfish bacteria generally dominate in the initial bloom stages, but a greater supply of increasingly complex substrates in later bloom stages leads to external hydrolysis of a wider range of substrates, increasing the supply of LMW hydrolysis products to the wider bacterial community.

Phytoplankton exudates and lysates support distinct microbial consortia with specialized metabolic and ecophysiological traits

“…The synthesis of these findings generally agrees with previous observations that Bacteroidetes populations increase in relative abundance and cell-specific activity in the middle and late phases of phytoplankton blooms and encode a large number of specialized enzymes allowing for the degradation and assimilation of polysaccharides ( 17 , 26 , 53 , 55 – 58 ). Our data further suggest that lysate DOM, particularly those derived from diatoms, stimulate higher cellular growth rates in Bacteroidetes taxa relative to other co-occurring populations and other substrates we tested, allowing this lineage to translate their resource use strategy into growth and division in a suitable environment.…”

“…Both peroxiredoxin enzymes and biopolymer transporters assigned to the Bacteroidetes became enriched in all substrate treatments, except for the cyanobacteria exudate treatment, implying that cells of this lineage are particularly well-suited for growth in the phycosphere, where oxygen levels and mucilage will be highest. The synthesis of these findings generally agrees with previous observations that Bacteroidetes populations increase in relative abundance and cell-specific activity in the middle and late phases of phytoplankton blooms and encode a large number of specialized enzymes allowing for the degradation and assimilation of polysaccharides (17,26,53,(55)(56)(57)(58). Our data further suggest that lysate DOM, particularly those derived from diatoms, stimulate higher cellular growth rates in Bacteroidetes taxa relative to other co-occurring populations and other substrates we tested, allowing this lineage to translate their resource use strategy into growth and division in a suitable environment.…”

Changing expression patterns of TonB-dependent transporters suggest shifts in polysaccharide consumption over the course of a spring phytoplankton bloom

“…1, data previously published in ref. [71]), implying a longer bloom than has been observed in prior years [5]. The composition of the algal community was similar to prior years [5], being dominated by diatoms (Supplementary Fig.…”

Quantifying fluorescent glycan uptake to elucidate strain-level variability in foraging behaviors of rumen bacteria

“…This event would increase the richness of the community and, potentially, result in the generation of additional secondary metabolites that benefit the lifestyle of MGs. Furthermore, it has been shown that both the concentrations and complexity of available substrate cause differential selection of distributive or selfish foraging strategies [47][48][49].…”