Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA.
Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA.
mBio. 2024 May 8;15(5):e0049624. doi: 10.1128/mbio.00496-24. Epub 2024 Mar 27.
Coastal herbivorous fishes consume macroalgae, which is then degraded by microbes along their digestive tract. However, there is scarce genomic information about the microbiota that perform this degradation. This study explores the potential of gastrointestinal microbial symbionts to collaboratively degrade and ferment polysaccharides from red, green, and brown macroalgae through study of carbohydrate-active enzyme and sulfatase sequences. Recovery of metagenome-assembled genomes (MAGs) from previously described gut metagenomes and newly sequenced bioreactor enrichments reveals differences in enzymatic capabilities between the major microbial taxa in guts. The most versatile of the recovered MAGs were from the phylum, whose MAGs house enzyme collections able to decompose a variety of algal polysaccharides. Unique enzymes and predicted degradative capacities of genomes from the (genus ) and (order ) highlight the importance of metabolic contributions from multiple phyla to broaden polysaccharide degradation capabilities. Few genomes contain the required enzymes to fully degrade any complex sulfated algal polysaccharide alone. The distribution of suitable enzymes between MAGs originating from different taxa, along with the widespread detection of signal peptides in candidate enzymes, is consistent with cooperative extracellular degradation of these carbohydrates. This study leverages genomic evidence to reveal an untapped diversity at the enzyme and strain level among symbionts and their contributions to macroalgae decomposition. Bioreactor enrichments provide a genomic foundation for degradative and fermentative processes central to translating the knowledge gained from this system to the aquaculture and bioenergy sectors.IMPORTANCESeaweed has long been considered a promising source of sustainable biomass for bioenergy and aquaculture feed, but scalable industrial methods for decomposing terrestrial compounds can struggle to break down seaweed polysaccharides efficiently due to their unique sulfated structures. Fish of the genus feed on seaweed by leveraging gastrointestinal bacteria to degrade algal polysaccharides into simple sugars. This study reconstructs metagenome-assembled genomes for these gastrointestinal bacteria to enhance our understanding of herbivorous fish digestion and fermentation of algal sugars. Investigations at the gene level identify guts as an untapped source of seaweed-degrading enzymes ripe for further characterization. These discoveries set the stage for future work incorporating marine enzymes and microbial communities in the industrial degradation of algal polysaccharides.
沿海草食性鱼类以大型藻类为食，这些藻类随后在其消化道内被微生物降解。然而，关于执行这种降解的微生物群落的基因组信息却很少。本研究通过研究碳水化合物活性酶和硫酸盐酶序列，探索了胃肠道微生物共生体协同降解和发酵红藻、绿藻和褐藻中多糖的潜力。从先前描述的肠道宏基因组和新测序的生物反应器富集物中回收宏基因组组装基因组（MAG），揭示了肠道中主要微生物类群之间在酶能力上的差异。从门中回收的 MAG 最为通用，其 MAG 中含有能够分解多种藻类多糖的酶集合。属和目（order ）的基因组中独特的酶和预测的降解能力突出了多个门的代谢贡献对于拓宽多糖降解能力的重要性。很少有基因组包含单独完全降解任何复杂硫酸化藻类多糖所需的酶。不同类群来源的 MAG 之间合适酶的分布，以及候选酶中广泛存在的信号肽，与这些碳水化合物的协同细胞外降解一致。本研究利用基因组证据揭示了共生体在酶和菌株水平上尚未开发的多样性，以及它们对大型藻类分解的贡献。生物反应器富集物为降解和发酵过程提供了基因组基础，这些过程是将从该系统获得的知识转化为水产养殖和生物能源部门的关键。重要性海藻长期以来一直被认为是生物能源和水产养殖饲料可持续生物量的有前途的来源，但由于其独特的硫酸化结构，可扩展的用于分解陆地化合物的工业方法在有效地分解海藻多糖方面可能会遇到困难。属的鱼类通过利用胃肠道细菌将藻类多糖降解成单糖来食用海藻。本研究重建了这些胃肠道细菌的宏基因组组装基因组，以增强我们对草食性鱼类消化和发酵藻类糖的理解。基因水平的研究确定肠道是海洋藻类降解酶的未开发来源，这些酶适合进一步表征。这些发现为未来的工作奠定了基础，即将海洋酶和微生物群落纳入藻类多糖的工业降解中。
