Herbivorous Fish Microbiome Adaptations to Sulfated Dietary Polysaccharides

Herbivorous Fish Microbiome Adaptations to Sulfated Dietary Polysaccharides
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DOI:
10.1128/aem.02154-22
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发表时间:
2023-05
影响因子:
4.4
通讯作者:
S. Podell;A. Oliver;L. Kelly;Wesley J. Sparagon;Alvaro M. Plominsky;R. Nelson;L. Laurens;Simona Augy
S. Podell;A. Oliver;L. Kelly;Wesley J. Sparagon;Alvaro M. Plominsky;R. Nelson;L. Laurens;Simona Augy
中科院分区:
生物学2区
文献类型:
--
作者:
S. Podell;A. Oliver;L. Kelly;Wesley J. Sparagon;Alvaro M. Plominsky;R. Nelson;L. Laurens;Simona Augy

文献摘要

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这项工作将特定的未培养的细菌类群与其海洋脊椎动物宿主中缺乏的不同多糖消化能力联系起来,为解构复杂的硫酸多糖和微生物获得扩大的大型藻类利用基因功能的潜在进化机制提供了新的见解。已经鉴定了数千种新的用于多糖利用的海洋特异性候选酶序列。海洋草食性鱼类主要以大型藻类为食,如Kyphosus属,它们对维持热带珊瑚礁的健康和丰富是必不可少的。在这里,深度宏基因组测序和组装的肠道隔室特定的样品从三个同域,macroalgivorous夏威夷kyphosid物种已被用来连接宿主肠道微生物类群与预测的蛋白质功能能力可能有助于有效的macroalgae消化。细菌群落组成,藻类的饮食来源,并预测酶的功能进行了分析,在平行的16个宏基因组跨越中,后肠消化区域的野生捕捞鱼类。在组装的重叠群上的扩展碳水化合物(CAZy)和硫酸酯酶(SulfAtlas)消化酶家族的基因共定位模式用于鉴定可能的多糖利用位点关联,并可视化针对复杂硫酸化多糖的细胞外输出蛋白的潜在合作网络。这些对草食性海洋鱼类肠道微生物群及其功能能力的见解提高了我们对消化复杂大型藻类硫酸多糖所涉及的酶和微生物的理解。重要性这项工作连接特定的未培养的细菌类群与不同的多糖消化能力缺乏海洋脊椎动物宿主,提供了新的见解到知之甚少的过程解构复杂的硫酸多糖和潜在的进化机制微生物收购扩大的大型藻类利用基因功能。已经鉴定了数千种新的用于多糖利用的海洋特异性候选酶序列。这些数据为今后研究珊瑚礁大型藻类过度生长的抑制、鱼类宿主生理学、在陆地和水产养殖动物饲料中使用大型藻类原料以及将大型藻类生物质生物转化为增值商业燃料和化学产品提供了基础资源。
This work connects specific uncultured bacterial taxa with distinct polysaccharide digestion capabilities lacking in their marine vertebrate hosts, providing fresh insights into poorly understood processes for deconstructing complex sulfated polysaccharides and potential evolutionary mechanisms for microbial acquisition of expanded macroalgal utilization gene functions. Several thousand new marine-specific candidate enzyme sequences for polysaccharide utilization have been identified. ABSTRACT Marine herbivorous fish that feed primarily on macroalgae, such as those from the genus Kyphosus, are essential for maintaining coral health and abundance on tropical reefs. Here, deep metagenomic sequencing and assembly of gut compartment-specific samples from three sympatric, macroalgivorous Hawaiian kyphosid species have been used to connect host gut microbial taxa with predicted protein functional capacities likely to contribute to efficient macroalgal digestion. Bacterial community compositions, algal dietary sources, and predicted enzyme functionalities were analyzed in parallel for 16 metagenomes spanning the mid- and hindgut digestive regions of wild-caught fishes. Gene colocalization patterns of expanded carbohydrate (CAZy) and sulfatase (SulfAtlas) digestive enzyme families on assembled contigs were used to identify likely polysaccharide utilization locus associations and to visualize potential cooperative networks of extracellularly exported proteins targeting complex sulfated polysaccharides. These insights into the gut microbiota of herbivorous marine fish and their functional capabilities improve our understanding of the enzymes and microorganisms involved in digesting complex macroalgal sulfated polysaccharides. IMPORTANCE This work connects specific uncultured bacterial taxa with distinct polysaccharide digestion capabilities lacking in their marine vertebrate hosts, providing fresh insights into poorly understood processes for deconstructing complex sulfated polysaccharides and potential evolutionary mechanisms for microbial acquisition of expanded macroalgal utilization gene functions. Several thousand new marine-specific candidate enzyme sequences for polysaccharide utilization have been identified. These data provide foundational resources for future investigations into suppression of coral reef macroalgal overgrowth, fish host physiology, the use of macroalgal feedstocks in terrestrial and aquaculture animal feeds, and the bioconversion of macroalgae biomass into value-added commercial fuel and chemical products.