Abstract：
The role of bacterial symbionts that populate octocorals (Cnidaria, Octocorallia) is still poorly understood. To shed light on their metabolic capacities, we examined 66 high-quality metagenome-assembled genomes (MAGs) spanning 30 prokaryotic species, retrieved from microbial metagenomes of three octocoral species and seawater.
Symbionts of healthy octocorals were affiliated with the taxa Endozoicomonadaceae, Candidatus Thioglobaceae, Metamycoplasmataceae, unclassified Pseudomonadales, Rhodobacteraceae, unclassified Alphaproteobacteria and Ca. Rhabdochlamydiaceae. Phylogenomics inference revealed that the Endozoicomonadaceae symbionts uncovered here represent two species of a novel genus unique to temperate octocorals, here denoted Ca. Gorgonimonas eunicellae and Ca. Gorgonimonas leptogorgiae. Their genomes revealed metabolic capacities to thrive under suboxic conditions and high gene copy numbers of serine-threonine protein kinases, type 3-secretion system, type-4 pili, and ankyrin-repeat proteins, suggesting excellent capabilities to colonize, aggregate, and persist inside their host. Contrarily, MAGs obtained from seawater frequently lacked symbiosis-related genes. All Endozoicomonadaceae symbionts harbored endo-chitinase and chitin-binging protein-encoding genes, indicating that they can hydrolyze the most abundant polysaccharide in the oceans. Other symbionts, including Metamycoplasmataceae and Ca. Thioglobaceae, may assimilate the smaller chitin oligosaccharides resulting from chitin breakdown and engage in chitin deacetylation, respectively, suggesting possibilities for substrate cross-feeding and a role for the coral microbiome in overall chitin turnover. We also observed sharp differences in secondary metabolite production potential between symbiotic lineages. Specific Proteobacteria taxa may specialize in chemical defense and guard other symbionts, including Endozoicomonadaceae, which lack such capacity.
This is the first study to recover MAGs from dominant symbionts of octocorals, including those of so-far unculturable Endozoicomonadaceae, Ca. Thioglobaceae and Metamycoplasmataceae symbionts. We identify a thus-far unanticipated, global role for Endozoicomonadaceae symbionts of corals in the processing of chitin, the most abundant natural polysaccharide in the oceans and major component of the natural zoo- and phytoplankton feed of octocorals. We conclude that niche partitioning, metabolic specialization, and adaptation to low oxygen conditions among prokaryotic symbionts likely contribute to the plasticity and adaptability of the octocoral holobiont in changing marine environments. These findings bear implications not only for our understanding of symbiotic relationships in the marine realm but also for the functioning of benthic ecosystems at large. Video Abstract.
Symbionts of healthy octocorals were affiliated with the taxa Endozoicomonadaceae, Candidatus Thioglobaceae, Metamycoplasmataceae, unclassified Pseudomonadales, Rhodobacteraceae, unclassified Alphaproteobacteria and Ca. Rhabdochlamydiaceae. Phylogenomics inference revealed that the Endozoicomonadaceae symbionts uncovered here represent two species of a novel genus unique to temperate octocorals, here denoted Ca. Gorgonimonas eunicellae and Ca. Gorgonimonas leptogorgiae. Their genomes revealed metabolic capacities to thrive under suboxic conditions and high gene copy numbers of serine-threonine protein kinases, type 3-secretion system, type-4 pili, and ankyrin-repeat proteins, suggesting excellent capabilities to colonize, aggregate, and persist inside their host. Contrarily, MAGs obtained from seawater frequently lacked symbiosis-related genes. All Endozoicomonadaceae symbionts harbored endo-chitinase and chitin-binging protein-encoding genes, indicating that they can hydrolyze the most abundant polysaccharide in the oceans. Other symbionts, including Metamycoplasmataceae and Ca. Thioglobaceae, may assimilate the smaller chitin oligosaccharides resulting from chitin breakdown and engage in chitin deacetylation, respectively, suggesting possibilities for substrate cross-feeding and a role for the coral microbiome in overall chitin turnover. We also observed sharp differences in secondary metabolite production potential between symbiotic lineages. Specific Proteobacteria taxa may specialize in chemical defense and guard other symbionts, including Endozoicomonadaceae, which lack such capacity.
This is the first study to recover MAGs from dominant symbionts of octocorals, including those of so-far unculturable Endozoicomonadaceae, Ca. Thioglobaceae and Metamycoplasmataceae symbionts. We identify a thus-far unanticipated, global role for Endozoicomonadaceae symbionts of corals in the processing of chitin, the most abundant natural polysaccharide in the oceans and major component of the natural zoo- and phytoplankton feed of octocorals. We conclude that niche partitioning, metabolic specialization, and adaptation to low oxygen conditions among prokaryotic symbionts likely contribute to the plasticity and adaptability of the octocoral holobiont in changing marine environments. These findings bear implications not only for our understanding of symbiotic relationships in the marine realm but also for the functioning of benthic ecosystems at large. Video Abstract.
摘要：
细菌共生体在八珊瑚中的作用（Cnidaria，Octocorallia）仍然知之甚少。为了揭示它们的代谢能力，我们检查了66个高质量的宏基因组组装基因组（MAG），跨越30个原核物种，从三种八珊瑚和海水的微生物宏基因组中回收。
健康的八珊瑚的共生体与类群内生虫科有关，念珠菌硫球蛋白科,变质科，未分类的假单胞菌，红杆菌科，未分类的α变形杆菌和钙。横纹肌科。系统发育组学推断表明，此处发现的Endozoicomonadaceae共生体代表了温带八珊瑚特有的新属的两个物种，这里表示Ca。海藻和钙。羊毛虫。他们的基因组揭示了在低氧条件下和高基因拷贝数的丝氨酸-苏氨酸蛋白激酶的代谢能力，3型分泌系统，4型菌毛，和锚蛋白重复蛋白，暗示了优秀的殖民能力，骨料,并坚持在他们的主人里面。相反，从海水中获得的MAG通常缺乏共生相关基因。所有内生子科共生体都带有内几丁质酶和几丁质结合蛋白编码基因，表明它们可以水解海洋中最丰富的多糖。其他共生体,包括后生菌科和Ca。硫球蛋白科，可能会吸收几丁质分解产生的较小的几丁质寡糖，并参与几丁质脱乙酰，分别,提示底物交叉进食的可能性以及珊瑚微生物组在整体甲壳素周转中的作用。我们还观察到共生谱系之间次生代谢产物产生潜力的明显差异。特定的变形杆菌类群可能专注于化学防御和保护其他共生体，包括内生子科，缺乏这种能力。
这是第一项从八角珊瑚的优势共生体中恢复MAG的研究，包括到目前为止无法培养的内生科，Ca.硫球蛋白科和后生孢子科共生体。我们发现了一个迄今为止意想不到的，珊瑚的内生共生体在甲壳素加工中的全球作用，海洋中最丰富的天然多糖，也是八角珊瑚的天然动物和浮游植物饲料的主要成分。我们得出的结论是，生态位划分，代谢专业化，原核共生体对低氧条件的适应可能有助于八珊瑚全体在不断变化的海洋环境中的可塑性和适应性。这些发现不仅对我们对海洋领域共生关系的理解，而且对整个底栖生态系统的功能都有影响。视频摘要。
健康的八珊瑚的共生体与类群内生虫科有关，念珠菌硫球蛋白科,变质科，未分类的假单胞菌，红杆菌科，未分类的α变形杆菌和钙。横纹肌科。系统发育组学推断表明，此处发现的Endozoicomonadaceae共生体代表了温带八珊瑚特有的新属的两个物种，这里表示Ca。海藻和钙。羊毛虫。他们的基因组揭示了在低氧条件下和高基因拷贝数的丝氨酸-苏氨酸蛋白激酶的代谢能力，3型分泌系统，4型菌毛，和锚蛋白重复蛋白，暗示了优秀的殖民能力，骨料,并坚持在他们的主人里面。相反，从海水中获得的MAG通常缺乏共生相关基因。所有内生子科共生体都带有内几丁质酶和几丁质结合蛋白编码基因，表明它们可以水解海洋中最丰富的多糖。其他共生体,包括后生菌科和Ca。硫球蛋白科，可能会吸收几丁质分解产生的较小的几丁质寡糖，并参与几丁质脱乙酰，分别,提示底物交叉进食的可能性以及珊瑚微生物组在整体甲壳素周转中的作用。我们还观察到共生谱系之间次生代谢产物产生潜力的明显差异。特定的变形杆菌类群可能专注于化学防御和保护其他共生体，包括内生子科，缺乏这种能力。
这是第一项从八角珊瑚的优势共生体中恢复MAG的研究，包括到目前为止无法培养的内生科，Ca.硫球蛋白科和后生孢子科共生体。我们发现了一个迄今为止意想不到的，珊瑚的内生共生体在甲壳素加工中的全球作用，海洋中最丰富的天然多糖，也是八角珊瑚的天然动物和浮游植物饲料的主要成分。我们得出的结论是，生态位划分，代谢专业化，原核共生体对低氧条件的适应可能有助于八珊瑚全体在不断变化的海洋环境中的可塑性和适应性。这些发现不仅对我们对海洋领域共生关系的理解，而且对整个底栖生态系统的功能都有影响。视频摘要。
