Grazers affect the composition of dissolved storage glycans and thereby bacterioplankton composition during a biphasic North Sea spring algae bloom

Abstract

Blooms of marine microalgae play a pivotal role in global carbon cycling. Such blooms entail successive blooms of specialized clades of planktonic bacteria that remineralize algal biomass. We investigated the bacterioplankton response to a bloom in the German Bight in spring 2020. Metagenome sequencing at 30 time-points allowed reconstruction of 251 metagenome-assembled genomes (MAGs), 245 representing as yet uncultured species, while corresponding metatranscriptome sequencing highlighted 50 particularly active MAGs. Together with algae, copepod, protist and bacteria diversity and abundance data in combination with physico-chemical data and antibody-based saccharide measurements, we demonstrate (i) how dissolved primary photoassimilated algal and secondary bacterial storage glycans shape the bacterioplankton community composition, and (ii) how grazing on higher trophic levels determines the release of these abundant glycans. We thus elucidate principles governing how bacterioplankton clades respond to algal blooms and collectively remineralize gigatons of carbon annually on a global scale.

Pulsed inputs of high molecular weight organic matter shift the mechanisms of substrate utilisation in marine bacterial communities

“…The ability to process αand β-linked glucans via external hydrolysis and/or selfish uptake is likely widespread among heterotrophic bacteria, due to the abundance of these polysaccharides in the ocean. Along these lines, a recent study has demonstrated that αand βglucan processing enzymes are widely and preferentially expressed by a broad phylogenetic range of bacteria during a spring phytoplankton bloom (Sidhu et al, 2023). Their target substrates are commonly available: annual oceanic production of laminarin has been estimated to be on the order of 5-15 billion metric tons (Alderkamp et al, 2007;Becker et al, 2020), and external hydrolysis of laminarin has been detected at almost every station and depth in the ocean surveyed to date (e.g., Arnosti et al, 2011;Balmonte et al, 2021).…”

Comparing genomes recovered from time-series metagenomes using long- and short-read sequencing technologies

“…During the spring of 2020, surface seawater samples were collected from the 'Kabeltonne' long-term ecological research station off the North Sea of Helgoland (54°11.3' N, 7°54.0' E) as described previously [13,14]. Surface water samples were collected on 2020-03-10, 2020-04-14, 2020-04-30, and 2020-05-06.…”

“…Metagenomes and MAGs data are available from the European Nucleotide Archive (ENA) project PRJEB52999 [14].…”

“…We sequenced DNA extracted from bacterioplankton collected in the 0.2-3 µm size fractions at four time points during the spring of 2020 in the North Sea. The sampling points comprised one pre-and three bloom events, part of a time-series sampling campaign during 2020 [14]. The Illumina SR approach recovered an average of 36 Gbp per sample (~ 240 bp paired-end reads), while the CCS PacBio LR approach recovered an average of 12 Gbp per sample (~ 6 kbp CCS reads) (Table S1).…”

Novel laminarin-binding CBMs in multimodular proteins of marineBacteroidotafeature prominently in phytoplankton blooms

“…Due to its abundance, water solubility and simple structure, marine bacteria often prefer laminarin as a substrate over less soluble and more complex polysaccharides (4,5). Polysaccharide utilization loci (PULs) dedicated to laminarin breakdown are thus both widely distributed (6,7) and are highly expressed (4,(8)(9)(10) in marine bacteria that thrive during phytoplankton blooms. PULs are distinct genetic loci that encode proteins to sense, digest and transport sugars.…”