Adaptive mechanisms that provide competitive advantages to marine bacteroidetes during microalgal blooms

Abstract

Polysaccharide degradation by heterotrophic microbes is a key process within Earth’s carbon cycle. Here, we use environmental proteomics and metagenomics in combination with cultivation experiments and biochemical characterizations to investigate the molecular details of in situ polysaccharide degradation mechanisms during microalgal blooms. For this, we use laminarin as a model polysaccharide. Laminarin is a ubiquitous marine storage polymer of marine microalgae and is particularly abundant during phytoplankton blooms. In this study, we show that highly specialized bacterial strains of the Bacteroidetes phylum repeatedly reached high abundances during North Sea algal blooms and dominated laminarin turnover. These genomically streamlined bacteria of the genus Formosa have an expanded set of laminarin hydrolases and transporters that belonged to the most abundant proteins in the environmental samples. In vitro experiments with cultured isolates allowed us to determine the functions of in situ expressed key enzymes and to confirm their role in laminarin utilization. It is shown that laminarin consumption of Formosa spp. is paralleled by enhanced uptake of diatom-derived peptides. This study reveals that genome reduction, enzyme fusions, transporters, and enzyme expansion as well as a tight coupling of carbon and nitrogen metabolism provide the tools, which make Formosa spp. so competitive during microalgal blooms.

Alpha‐ and beta‐mannan utilization by marine Bacteroidetes

“…S6). These putative laminarin PULs encode glycoside hydrolases that have been previously shown to be involved in laminarin degradation by proteomics (Kabisch et al, 2014;Xing et al, 2015) and biochemical analyses (Labourel et al, 2014;Unfried et al, 2018). We therefore used laminarin degradation activity as a functionally characterized positive control.…”

Comparative genomics reveals complex natural product biosynthesis capacities and carbon metabolism across host‐associated and free‐living Aquimarina (Bacteroidetes, Flavobacteriaceae) species

“…Despite its quite recent discovery in 2005 (Nedashkovskaya et al, 2005), a wide range of bioactivities of putative relevance in the cycling of matter and establishment of hostmicrobe and microbe-microbe relationships has lately been reported for a few Aquimarina strains. Besides showing a versatile carbon metabolism typical of members of the family Flavobacteriaceae and, in a broader sense, of the phylum Bacteroidetes (Alonso et al, 2007;Boone et al, 2010;Fernández-Gómez et al, 2013;Unfried et al, 2018), these organisms have been matter of current research attention owing to metabolic features of both ecological and biotechnological interest. For instance, Aquimarina salinaria (Chen et al, 2012) was shown to possess antagonistic activity towards the toxic cyanobacterium Microcystis aeruginosa (Chen et al, 2011;Chen et al, 2012).…”

FGB1 and WSC3 are in planta‐induced β‐glucan‐binding fungal lectins with different functions

“…This reaction leads to glucose and the linear b1-3-glucan. Completeness of the conversion was confirmed by testing the activity of a b1-3endo glucanase of family GH17 that only cleaves undecorated, linear b1-3-glucan (Becker et al, 2017;Unfried et al, 2018) and shows little activity on the native yet high activity on the debranched laminarin. The reaction was stopped by boiling the sample for 5 min at 100°C.…”

“…The solution was dried in vacuum overnight at 45°C to obtain a white powder. The enzymatic digestion with both enzymes and absence of glucose in the final product was recorded by high performance anionic exchange chromatography with pulsed amperometric detection (HPAEC-PAD) on a Dionex system (Unfried et al, 2018).…”

“…strain B. This enzyme was previously shown to specifically hydrolyze the b1-6-linked glucose side chains of laminarin (K M : 3.1 AE 0.2 mM and K cat /K M : 21124 M À1 s À1 ) producing linear b1-3-glucan (Becker et al, 2017;Unfried et al, 2018). The MST analysis at pH 5 showed that whereas FGB1 binds to native laminarin this lectin does not bind to debranched laminarin.…”