Fucoidan degradation by marine bacteria

Abstract

The oceans are an important carbon sink that have sequestered about half of all anthropogenic CO2 emissions. Marine carbon cycling is driven by the deposition of photosynthetic micro- and macroalgae in ocean sediments, where carbon is stored over thousands of years. The algal polysaccharide fucoidan is considered to be recalcitrant to microbial degradation and may therefore facilitate long-term carbon storage. Yet, factors that render fucoidan recalcitrant against microbial degradation remain unidentified, hampering our understanding of fucoidans in the carbon cycle. Fucoidans originating from the cell wall of brown algae are often co-extracted with other cell wall components. In Chapter I, I develop a simple step-wise protocol to purify fucoidans from different brown algae. Using mass spectrometry and nuclear magnetic resonance analyses, I describe the highly diverse and branched structures of different fucoidans. In Chapter II, I examine how marine bacteria degrade those complex branched fucoidans. Using genomics, proteomics and biochemistry, I characterize the newly isolated Verrucomicrobium a Lentimonasa sp. CC4 and show that fucoidan degradation requires highly dedicated pathways of over 100 enzymes covering 20% of the a Lentimonasa sp. CC4 proteome. The complexity of these pathways implies that only highly specialized bacteria can effectively degrade fucoidans and gives a clue why it may be recalcitrant. The proteomic analysis of a Lentimonasa sp. CC4 in chapter II suggested that two protein families, S1 15 and GH29, are key in fucoidan degradation. In Chapter III, I biochemically and structurally characterize one S1 15 sulfatase and one GH29 fucosidase, revealing their exo-enzyme activity and a novel catalytic pair of two aspartate residues. This provides insights into the molecular mechanism of exo-enzymatic fucoidan degradation. In Chapter IV, I trace the dynamics of different polysaccharides during a diatom spring bloom in Helgoland. I found that the dominant bloom-forming diatom Chaetoceros socialis secretes fucoidan in dissolved form, which aggregates and accumulates in particles at the end of the bloom. Known enzymes to degrade this polysaccharide are not expressed in the microbial community which indicates that fucoidans are not microbially degraded and act as vector for organic carbon drawdown. To summarize, fucoidans are diverse, highly branched polysaccharides whose degradation requires a large set of enzymes found in very few specialized marine bacteria. Their stability-enhancing properties lead to increased brown algal deposition in coastal sediments and in the open ocean they may acts as aggregation nuclei that enhance aggregation and settling of phytoplankton aggregates. Their abundance, recalcitrant nature and stickiness make fucoidans a likely key players in oceanic carbon sequestration.