X-STAR, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan.
College of Science and Engineering, Kanazawa University, Kanazawa, Japan.
Appl Environ Microbiol. 2022 Apr 26;88(8):e0018522. doi: 10.1128/aem.00185-22. Epub 2022 Apr 11.
Hydrothermal vent ecosystems are home to a wide array of symbioses between animals and chemosynthetic microbes, among which shrimps in the genus Rimicaris is one of the most iconic. So far, studies of symbioses have been restricted to Atlantic species, including Rimicaris exoculata, which is totally reliant on the symbionts for nutrition, and the mixotrophic species Rimicaris chacei. Here, we expand this by investigating and characterizing the symbiosis of the Indian Ocean species Rimicaris kairei using specimens from two vent fields, Kairei and Edmond. We also aimed to evaluate the differences in mineralogy and microbial communities between two cephalothorax color morphs, black and brown, through a combination of 16S metabarcoding, scanning electron microscopy, fluorescent hybridization, energy-dispersive X-ray spectroscopy, and synchrotron near-edge X-ray absorption structure analyses. Overall, our results highlight that R. kairei exhibits similar symbiont lineages to those of its Atlantic congeners, although with a few differences, such as the lack of Zetaproteobacteria. We found distinct mineralization processes behind the two color morphs that were linked to differences in the vent fluid composition, but the symbiotic community composition was surprisingly similar. In R. exoculata, such mineralogical differences have been shown to stem from disparity in the microbial communities, but our results indicate that in this is instead due to the shift of dominant metabolisms by the same symbiotic partners. We suggest that a combination of local environmental factors and biogeographic barriers likely contribute to the differences between Atlantic and Indian Ocean symbioses. Hydrothermal vent shrimps in the genus are among the most charismatic deep-sea animals of Atlantic and Indian Oceans, often occurring on towering black smokers in dense aggregates of thousands of individuals. Although this dominance is only possible because of symbiosis, no study on the symbiosis of Indian Ocean species has been conducted. Here, we characterize the symbiosis by combining molecular, microscopic, and elemental analyses, making comparisons with those of the Atlantic species possible for the first time. Although most symbiotic partners remained consistent across the two oceans, some differences were recognized in symbiont lineages, as well as in the mechanisms behind the formation of two color morphs with distinct mineralogies. Our results shed new light on relationships among mineralogy, environmental factors, and microbial communities that are useful for understanding other deep-sea symbioses in the future.
热液喷口生态系统是动物和化学合成微生物之间广泛共生的家园，其中虾属 Rimicaris 是最具代表性的一种。到目前为止，共生的研究仅限于大西洋物种，包括完全依赖共生体获取营养的 Rimicaris exoculata 和混合营养物种 Rimicaris chacei。在这里，我们通过研究来自两个喷口场（Kairei 和 Edmond）的印度洋洋中脊 Rimicaris kairei 标本，扩展了这一研究。我们还旨在通过结合 16S 代谢组学、扫描电子显微镜、荧光杂交、能量色散 X 射线光谱和同步辐射近边缘 X 射线吸收结构分析，评估两种头胸甲颜色形态（黑色和棕色）之间在矿物学和微生物群落方面的差异。总的来说，我们的结果表明，R. kairei 表现出与大西洋同属物种相似的共生体谱系，尽管存在一些差异，例如缺乏 Zetaproteobacteria。我们发现两种颜色形态背后存在不同的矿化过程，这与喷口流体成分的差异有关，但共生体群落组成却惊人地相似。在 R. exoculata 中，这种矿物学差异是由微生物群落的差异引起的，但我们的结果表明，这是由于相同共生体伙伴的主要代谢途径发生了转变。我们认为，局部环境因素和生物地理屏障的结合可能导致大西洋和印度洋共生体之间的差异。虾属热液喷口虾是大西洋和印度洋最具魅力的深海动物之一，经常出现在高耸的黑烟囱上，密集地聚集着成千上万的个体。尽管这种优势只有通过共生才能实现，但对印度洋物种的共生关系还没有进行研究。在这里，我们通过结合分子、微观和元素分析来描述这种共生关系，使首次有可能与大西洋物种进行比较。尽管两个海洋中的大多数共生伙伴保持一致，但在共生体谱系以及两种具有不同矿物学特征的颜色形态形成的机制方面，我们也发现了一些差异。我们的研究结果为未来理解其他深海共生关系提供了有关矿物学、环境因素和微生物群落之间关系的新视角。
