Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia.
Proc Natl Acad Sci U S A. 2017 Sep 5;114(36):E7592-E7601. doi: 10.1073/pnas.1703070114. Epub 2017 Aug 23.
Herbivorous surgeonfishes are an ecologically successful group of reef fish that rely on marine algae as their principal food source. Here, we elucidated the significance of giant enteric symbionts colonizing these fishes regarding their roles in the digestive processes of hosts feeding predominantly on polysiphonous red algae and brown algae, which contain different polysaccharide constituents. Using metagenomics, single-cell genomics, and metatranscriptomic analyses, we provide evidence of metabolic diversification of enteric microbiota involved in the degradation of algal biomass in these fishes. The enteric microbiota is also phylogenetically and functionally simple relative to the complex lignocellulose-degrading microbiota of terrestrial herbivores. Over 90% of the enzymes for deconstructing algal polysaccharides emanate from members of a single bacterial lineage, " Epulopiscium" and related giant bacteria. These symbionts lack cellulases but encode a distinctive and lineage-specific array of mostly intracellular carbohydrases concurrent with the unique and tractable dietary resources of their hosts. Importantly, enzymes initiating the breakdown of the abundant and complex algal polysaccharides also originate from these symbionts. These are also highly transcribed and peak according to the diel lifestyle of their host, further supporting their importance and host-symbiont cospeciation. Because of their distinctive genomic blueprint, we propose the classification of these giant bacteria into three candidate genera. Collectively, our findings show that the acquisition of metabolically distinct "" symbionts in hosts feeding on compositionally varied algal diets is a key niche-partitioning driver in the nutritional ecology of herbivorous surgeonfishes.
草食性医生鱼是一类在生态上非常成功的珊瑚礁鱼类，它们主要以海洋藻类为食。在这里，我们阐明了定植在这些鱼类肠道中的巨型共生菌的重要性，这些共生菌在以多枝红藻和褐藻为主食的鱼类的消化过程中发挥作用，而这些藻类含有不同的多糖成分。通过宏基因组学、单细胞基因组学和宏转录组学分析，我们为肠道微生物群在降解这些鱼类主要以多糖为主的藻类生物质方面的代谢多样化提供了证据。与陆地草食动物复杂的木质纤维素降解微生物群相比，肠道微生物群在系统发育和功能上也相对简单。超过 90%的用于分解藻类多糖的酶来自一个单一的细菌谱系“Epulopiscium”和相关的巨型细菌。这些共生菌缺乏纤维素酶，但编码一组独特的、具有种系特异性的、主要是细胞内的水解酶，与它们宿主独特且易于处理的饮食资源相匹配。重要的是，启动丰富而复杂的藻类多糖分解的酶也来源于这些共生菌。这些酶的转录水平也很高，并根据宿主的昼夜生活方式达到峰值，进一步支持了它们的重要性和宿主-共生菌共进化。由于它们独特的基因组蓝图，我们建议将这些巨型细菌分类为三个候选属。总的来说，我们的研究结果表明，在以成分多样的藻类为食的宿主中获得代谢上不同的“共生菌”是草食性医生鱼营养生态学中关键的生态位分化驱动因素。
