Cleaning stations as hubs for the maintenance and recovery of microbial diversity on coral reefs. Cleanerfish microbiomes

Biodiversity in the ocean is influenced by interactions between disparate organisms which ultimately shape population, community, and ecosystem dynamics. Symbiotic interactions involving subsets of species can have disproportionate impacts on communities, reaching well beyond each interacting species. Coral reefs host some of the most iconic symbiotic interactions in nature and are host to the highest diversity of life on the planet. Cleaning symbiosis, wherein small fish or shrimp remove external parasites and associated microorganisms from specific clients, is common on coral reefs. Sites on the reef occupied by cleaners, or "cleaning stations", attract a wide variety of fish species that engage in direct physical contact with the cleaner. These highly used territories are viewed both as "clinics of the sea", where parasitized and sickly fish seek the service of cleaners, but also as potential "garbage dumps", where unnecessary parasites and other microorganisms are removed. This project seeks to understand the role of cleaning symbiosis transferring microbes in coral reef environments. This research supports training for U.S. graduate students and for undergraduates from Arkansas State University, a primarily undergraduate institution that includes a large population of first-generation college students. These students participate in field site research and have opportunities to visit the Woods Hole Oceanographic Institution for broader exposure to ocean science and more specific laboratory training. The project strengthens international collaboration and further builds on the existing relationships between the team of scientists and resource managers, local divers, fishers, and boat operators, as well as K-12 schools and environmental education programs, and will therefore contribute to local economies. Outreach efforts include a film highlighting this research and publicly accessible narratives shared through press releases and an on-line magazine.While the benefits of cleaning to reef ecosystem health have been extensively studied, the cleaning costs for cleaner species and the role of cleaning stations as potential sinks for microbial diversity and possibly even pathogens have never been assessed. Here, the researchers utilize the unique features of cleaning stations to understand transfer of bacterial and archaeal symbionts amongst fish and within coral reef environment. The study capitalizes on cleanerfish access to multiple variety of hosts or clients within stations to address new questions about how cleanerfish act as vectors to transfer microorganisms between hosts on a reef and if and how these microorganisms may play a broader functional role in reef resilience. Specifically, the project addresses the following hypotheses: 1) Cleanerfishes serve as keystone regulators of microbial communities, enhancing microbial community diversity and transferring key microbial species between clients, and 2) Cleanerfishes are a particularly important contributor to reef resilience, facilitating recovery of the microbiome following disturbance. The research team uses an integrative interdisciplinary approach involving field and laboratory observations and experiments, and molecular-based tools. The core research team includes experts in cleaning mutualisms, fish behavior, coral reef ecology, and microbial ecology. The proposed project aims to link behavior of individual organisms with ecosystem-level process.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

海洋生物多样性由异源生物间的相互作用所调控，此类相互作用最终塑造了种群、群落与生态系统的动态变化。仅涉及部分物种类群的共生相互作用，可对群落产生远超参与互作物种本身的不成比例的显著效应。珊瑚礁承载着自然界中最具标志性的共生相互作用之一，同时也是全球生物多样性最为丰富的生境。清洁共生（cleaning symbiosis）在珊瑚礁中极为普遍，指小型鱼类或虾类从特定的客户鱼体表移除体外寄生虫及相关微生物的互作过程。珊瑚礁上被清洁者占据的区域，即“清洁站”，会吸引大量鱼类前来，这些鱼类会与清洁者发生直接的身体接触。这些高频使用的领地既被视为“海洋诊所”——受寄生虫侵染或患病的鱼类在此寻求清洁服务，同时也可被视作潜在的“垃圾场”——无用的寄生虫与其他微生物在此被清除。本项目旨在厘清清洁共生作用在珊瑚礁生境中参与微生物传播的具体功能。本研究为美国研究生及阿肯色州立大学（Arkansas State University）的本科生提供培训支持。阿肯色州立大学是一所侧重本科教育的院校，校内第一代大学生群体规模庞大。这些学生将参与野外实地研究，并有机会访问伍兹霍尔海洋研究所（Woods Hole Oceanographic Institution），以拓展海洋科学领域的视野并获得更具针对性的实验室训练。本项目将强化国际合作，并进一步巩固科研团队与资源管理者、当地潜水员、渔民、船运营商，以及K12学校与环境教育项目之间的既有合作关系，同时助力当地经济发展。科普推广工作包括制作聚焦本研究的纪录片，以及通过新闻稿与在线杂志发布面向公众的科普内容。尽管清洁共生对珊瑚礁生态系统健康的益处已得到广泛研究，但清洁物种所付出的清洁成本，以及清洁站作为微生物多样性乃至潜在病原体汇的功能，此前从未得到评估。本研究中，科研人员将利用清洁站的独特特征，探究鱼类之间以及珊瑚礁生境内部的细菌与古菌共生体传播过程。本研究依托清洁鱼在清洁站内可接触多种宿主（客户鱼）的特点，旨在解答两大新问题：其一，清洁鱼如何作为媒介在珊瑚礁的宿主之间传播微生物；其二，这些微生物是否以及如何在珊瑚礁韧性维持中发挥更广泛的功能作用。具体而言，本项目将验证以下两项假说：1. 清洁鱼是微生物群落的关键调控者，可提升微生物群落多样性，并在客户鱼之间传播关键微生物类群；2. 清洁鱼是维持珊瑚礁韧性的重要贡献者，可助力受干扰后珊瑚礁微生物组的恢复。科研团队将采用整合交叉学科研究方法，涵盖野外与实验室观测、实验操作及分子生物学技术手段。核心科研团队成员涵盖清洁共生互作、鱼类行为学、珊瑚礁生态学及微生物生态学领域的专家。本项目旨在将个体生物行为与生态系统级过程建立关联。本资助项目符合美国国家科学基金会（National Science Foundation, NSF）的法定使命，并通过了该基金会以“知识价值”与“广泛影响力”为评审标准的评估，被认定为具备资助价值。