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Polyelectrolyte mannan from diatoms reshapes sunlit ocean microbiome

Krull, J.; Crawford, C. J.; Sidhu, C.; Solanki, V.; Bligh, M.; Rössler, L.; Singh, R. K.; Huang, G.; Robb, C. S.; Teeling, H. J.; Seeberger, P. H.; Schweder, T.; Hehemann, J.-H.

2024-07-05 ecology
10.1101/2024.07.03.601839 bioRxiv
Show abstract

Diatoms are a keystone phylum in Earths ecosystems, specializing in oxygen production and carbohydrate fixation that fuels global food webs. Diatoms host a microbiome, but how they preferentially collect bacteria with complementary traits remains unknown. Here we show that diatoms exude a C6-sulfated -1,3-mannan that serves as a selective carbon source for adapted bacteria. Its structure was resolved by NMR spectroscopy, chromatography, chemical synthesis, and enzymatic dissection. Biochemical, physiological, and structural analyses revealed that specialized Bacteroidota employ a four-enzyme pathway to metabolize this mannan. Metagenomic and transcriptomic data indicate that the mannan globally selects for bacteria carrying these enzymes and associated traits. Because the mannan provides only carbon, oxygen, sulfur, and hydrogen, bacteria must obtain other essential elements from alternative sources, reinforcing metabolic interdependence. We propose that diatoms use sulfated mannans to attract beneficial partners and exclude competitors, thereby engineering a microbiome that enhances their productivity and underpins carbon cycling. Significance statementEukaryotes host microbial partners that shape their health, yet how they selectively assemble beneficial microbes remains unclear. Using diatom microalgae as a model, we show they exude a sulfated mannan that nourishes highly adapted bacteria tracking them across the global ocean. Our findings suggest that single-celled eukaryotes can "domesticate" prokaryotes--analogous to how humans have domesticated animals--albeit on a microscopic scale. Dominating much of Earths aquatic surface, diatoms drive [~]20% of global photosynthesis. We propose that sulfated mannan contributes to this success by helping diatoms shape microbial partnerships that underpin planetary energy balance and atmospheric chemistry.

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