Alpha-glucans from bacterial necromass indicate an intra-population loop within the marine carbon cycle

Abstract

Phytoplankton blooms provoke bacterioplankton blooms, from which bacterial biomass (necromass) is released via increased zooplankton grazing and viral lysis. While bacterial consumption of algal biomass during blooms is well-studied, little is known about the concurrent recycling of these substantial amounts of bacterial necromass. We demonstrate that bacterial biomass, such as bacterial alpha-glucan storage polysaccharides, generated from the consumption of algal organic matter, is reused and thus itself a major bacterial carbon source in vitro and during a diatom-dominated bloom. We highlight conserved enzymes and binding proteins of dominant bloom-responder clades that are presumably involved in the recycling of bacterial alpha-glucan by members of the bacterial community. We furthermore demonstrate that the corresponding protein machineries can be specifically induced by extracted alpha-glucan-rich bacterial polysaccharide extracts. This recycling of bacterial necromass likely constitutes a large-scale intra-population energy conservation mechanism that keeps substantial amounts of carbon in a dedicated part of the microbial loop.

Internal carbon recycling by heterotrophic prokaryotes compensates for mismatches between phytoplankton production and heterotrophic consumption

“…Fourth, a recent study from the Helgoland time series showed that bacteria not only expressed polysaccharide utilization loci for utilization of beta-glucans (produced by phytoplankton), but also for alpha-glucans (produced by bacteria), and the authors hypothesized that a recycling of bacterial glucans occurs [ 41 ]. This hypothesis was corroborated by follow-up results in the same time series showing that the phytoplankton storage polysaccharide laminarin fuels the synthesis of alpha-glucans in bacteria during phytoplankton blooms, and that these are used as a carbon source by other bacteria if liberated by cell lysis ([ 42 ], also see the SI for overlaps in the suggested taxonomy of important taxa between this and our study). The authors of that study conclude that large amounts of carbon may get redirected via an intrapopulation loop, which corroborates the outcomes of our mechanistic inference approach by metatranscriptomic analyses.…”

“…al. [ 42 ] suggests that the proposed internal recycling also takes place at other places in significant amounts, and we encourage future analyses of aquatic microbial communities to also resolve fluxes between heterotrophic prokaryotes. The assumption applied thus far that heterotrophic prokaryotes only consume DOM and do not also produce it for further consumption by others may be a gross oversimplification.…”