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bioRxiv · 10.1101/2024.12.10.627767

Resource partitioning in organosulfonate utilization by free-living heterotrophic bacteria during a North Sea microalgal bloom

Sidhu, C.·Bartosik, D.·Kale, V.·Trautwein-Schult, A.·Becher, D.·Schweder, T.·Amann, R.·Teeling, H.
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Abstract

Blooming microalgae (phytoplankton) release diverse organic molecules that fuel the marine pools of dissolved and particulate organic matter. A highly specialized community of heterotrophic bacteria rapidly remineralizes substantial parts of this organic matter in the sun-lit upper ocean. In particular, microalgae produce large quantities of various organosulfur compounds that can serve as carbon and sulfur sources for bacteria. Here, we report on the analyses of a time series of previously generated 30 long-read metagenomes, 30 corresponding deeply sequenced short-read metatranscriptomes and 15 metaproteomes from 0.2-3 {micro}m size fractions that we sampled in 2020 during a biphasic phytoplankton bloom in the German Bight (Southern North Sea). We analyzed the assembled contigs as well as 70 bacterial metagenome-assembled genomes that recruited the highest transcript numbers with respect to the utilization of methyl sulfur compounds (dimethylsulfoniopropionate (DMSP), dimethyl sulfide (DMS), dimethyl sulfone (DMSO2)), C3-sulfonates (2,3-dihydroxypropane-1-sulfonate (DHPS), 3-sulfolactate, 3-sulfopyruvate) and 2-aminoethanesulfonic acid (taurine). We observed a pronounced resource partitioning among bacterial clades that utilize distinct organosulfur compounds, which may explain successions of these clades during the studied bloom. Alphaproteobacteria were the most active and degraded a variety of organosulfonates via various metabolic routes. However, we also found previously underreported roles of members of the Bacteroidota and Gammaproteobacteria as efficient degraders of DMSP, DMS, and DMSO2. One striking observation was a strong preference for DMSP cleavage in Bacteroidota as opposed to DMSP demethylation in Alphaproteobacteria and indications for a particular proficiency for taurine utilization in Ilumatobacter_A and Acidimicrobiia. ImportanceSulfur-containing low-molecular-weight algal metabolites play an important role in overall marine carbon and sulfur fluxes. This study highlights that such compounds may play a crucial role in governing the succession of distinct bacterioplankton clades in response to phytoplankton blooms in coastal shelf areas of the temperate zone, such as the German Bight of the North Sea. While Alphaproteobacteria are the most versatile and competitive degraders of dissolved organosulfur compounds during such blooms, this study repositions clades previously thought to play only a more limited role in dissolved organosulfur metabolism in situ, such as Gammaproteobacteria, Bacteroidota, and Acidimicrobiia, as crucial contributors to the remineralization of organosulfur compounds in the upper ocean. This study also highlights the high level of interconnectedness of bacterial carbon and sulfur cycling during phytoplankton blooms.

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Sidhu, C., Bartosik, D., Kale, V., Trautwein-Schult, A., Becher, D., Schweder, T., Amann, R., Teeling, H.. 2024-12-16. Resource partitioning in organosulfonate utilization by free-living heterotrophic bacteria during a North Sea microalgal bloom. https://doi.org/10.1101/2024.12.10.627767

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