Project description:Macroalgae contribute substantially to primary production in coastal ecosystems. Their biomass, mainly consisting of polysaccharides, is cycled into the environment by marine heterotrophic bacteria (MHB), using largely uncharacterized mechanisms. In Zobellia galactanivorans, we discovered and characterized the complete catabolic pathway for carrageenans, major cell wall polysaccharides of red macroalgae, providing a model system for carrageenan utilization by MHB. We further demonstrate that carrageenan catabolism relies on a multifaceted carrageenan-induced regulon, including a non-canonical polysaccharide utilization locus (PUL) and several distal genes. The genetic structure of the carrageenan utilization system is well conserved in marine Bacteroidetes, but modified in other MHB phyla. The core system is completed by additional functions which can be assumed by non-orthologous genes in different species. This complex genetic structure is due to multiple evolutionary events including gene duplications and horizontal gene transfers. These results allow for an extension on the definition of bacterial PUL-mediated polysaccharide digestion.
Project description:Polysaccharides from macroalgae are important bacterial nutrient source and central biogeochemical component in the oceans. To illuminate the cellular mechanisms of polysaccharide degradation by marine bacteria, growth of Alteromonas macleodii 83-1 on a mix of laminarin, alginate and pectin was characterized using transcriptomics, proteomics and exometabolomics. A. macleodii 83-1 showed two distinct growth stages, with exponential growth during laminarin utilization followed by maintenance during simultaneous alginate/pectin utilization. The biphasic growth coincided with major temporal shifts in gene expression and metabolite secretion, enabling to define major/accessory polysaccharide utilization loci, reconstruct the complete degradation pathways for each polysaccharide, as well as identify temporal phenotypes in other relevant traits. FT-ICR-MS revealed a distinct suite of secreted metabolites for each growth phase, with pyrroloquinoline quinone exclusively produced with alginate/pectin. The finding of substrate-unique phenotypes indicates an exquisite adaptation to polysaccharide utilization with probable relevance for the degradation of macroalgal biomass, which comprises a complex mix of polysaccharides. Moreover, substrate-unique exometabolomes possibly influence metabolic interactions with other community members. Overall, the presence of fine-tuned genetic machineries for polysaccharide degradation and the widespread detection of related CAZymes in global locations indicate an ecological relevance of A. macleodii in marine polysaccharide cycling and bacteria-algae interactions.
Project description:Marine microalgae (phytoplankton) mediate almost half of the worldwide photosynthetic carbon dioxide fixation and therefore play a pivotal role in global carbon cycling, most prominently during massive phytoplankton blooms. Phytoplankton biomass consists of considerable proportions of polysaccharides, substantial parts of which are rapidly remineralized by heterotrophic bacteria. We analyzed the diversity, activity and functional potential of such polysaccharide-degrading bacteria in different size fractions during a diverse spring phytoplankton bloom at Helgoland Roads (southern North Sea) at high temporal resolution using microscopic, physicochemical, biodiversity, metagenome and metaproteome analyses.
Project description:Deconstruction is an essential step of conversion of polysaccharides, and polysaccharide-degrading enzymes play a key role in this process. Although there is recent progress in the identification of these enzymes, the diversity and phylogenetic distribution of these enzymes in marine microorganisms remain largely unknown, hindering our understanding of the ecological roles of marine microorganisms in the ocean carbon cycle. Here, we studied the phylogenetic distribution of nine types of polysaccharide-degrading enzymes in marine bacterial genomes. First, we manually compiled a reference sequence database containing 961 experimentally verified enzymes. With this reference database, we annotated 9,335 enzyme sequences from 2,182 high-quality marine bacterial genomes, revealing extended distribution for six enzymes at the phylum level and for all nine enzymes at lower taxonomic levels. Next, phylogenetic analyses revealed intra-clade diversity in the encoding potentials and phylogenetic conservation of a few enzymes at the genus level. Lastly, our analyses revealed correlations between enzymes, with alginate lyases demonstrating the most extensive correlations with others. Intriguingly, chitinases showed negative correlations with cellulases, alginate lyases, and agarases in a few genera. This result suggested that intra-genus lifestyle differentiation occurred many times in marine bacteria and that the utilization of polysaccharides may act as an important driver in the recent ecological differentiation of a few lineages. This study expanded our knowledge of the phylogenetic distribution of polysaccharide enzymes and provided insights into the ecological differentiation of marine bacteria.
Project description:Humans harbor numerous species of colonic bacteria that digest the fiber polysaccharides in commonly consumed terrestrial plants. More recently in history, regional populations have consumed edible seaweeds (macroalgae) containing unique polysaccharides. However, it remains unclear how extensively gut bacteria have adapted to digest these novel nutrients. Here, we show that the ability of gut bacteria to digest seaweed polysaccharides is considerably more pervasive than previously appreciated. Using culture-based approaches, we show that known Bacteroides genes involved in seaweed degradation have mobilized into many members of this genus. We also identify new marine bacteria-derived genes, and their corresponding mobile DNA elements, that are involved in degrading several seaweed polysaccharides. Some of these new genes reside in gut-resident, Gram-positive Firmicutes, for which phylogenetic analysis suggests an origin in the Epulopiscium gut symbionts of marine fishes. Our results are important for understanding the metabolic plasticity of the human gut microbiome, the global exchange of genes in the context of dietary selective pressures and identifying new functions that can be introduced or engineered to design and fill orthogonal niches for a future generation of engineered probiotics.