Human Impact on Symbioses Between Aquatic Organisms and Microbes
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Vol. 87: 113–138, 2021 AQUATIC MICROBIAL ECOLOGY Published online August 26 https://doi.org/10.3354/ame01973 Aquat Microb Ecol Contribution to AME Special 7 ‘SAME 16: Progress and perspectives in aquatic microbial ecology’ OPEN ACCESS REVIEW Human impact on symbioses between aquatic organisms and microbes Willem Stock1,2,#, Martijn Callens3,#, Shira Houwenhuyse4, Ruben Schols4,5, Naina Goel4,6, Manon Coone4, Charlotte Theys7, Vienna Delnat7, Alice Boudry4,7, Ester M. Eckert8, Cecilia Laspoumaderes9,10, Hans-Peter Grossart11,12, Luc De Meester7,13, Robby Stoks7, Koen Sabbe1, Ellen Decaestecker4,* 1Laboratory of Protistology & Aquatic Ecology, Department of Biology, Ghent University, 9000 Ghent, Belgium 2Phycology Research Group, Department of Biology, Ghent University, 9000 Ghent, Belgium 3CEFE, Univ Montpellier, CNRS, EPHE, IRD, Univ Paul Valéry Montpellier 3, 34080 Montpellier, France 4Laboratory of Aquatic Biology, KU Leuven Kulak, 8500 Kortrijk, Belgium 5Department of Biology, Royal Museum for Central Africa, 3080 Tervuren, Belgium 6Faculty of Bioscience Engineering, Department of Animal Sciences and Aquatic Ecology, University of Ghent, 8400 Oostende, Belgium 7Laboratory of Aquatic Ecology, Evolution and Conservation, KU Leuven, 3000 Leuven, Belgium 8Water Research Institute — National Research Council of Italy (CNR-IRSA), Molecular Ecology Group (MEG), 28922 Verbania, Italy 9Departamento de Ecología, Laboratorio de Limnología, INIBIOMA, CONICET-Universidad Nacional del Comahue, 8400 Bariloche, Argentina 10Alfred-Wegener-Institut Helmholtz-Zentrum für Polar- und Meeresforschung, Biologische Anstalt Helgoland, 27498 Helgoland, Germany 11Dept. of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), 16775 Stechlin, Germany 12Dept. of Biochemistry and Biology, Potsdam University, 14469 Potsdam, Germany 13Dept. of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), 12587 Berlin, Germany ABSTRACT: Aquatic organisms rely on microbial symbionts for coping with various challenges they encounter during stress and for defending themselves against predators, pathogens and para- sites. Microbial symbionts are also often indispensable for the host’s development or life cycle com- pletion. Many aquatic ecosystems are currently under pressure due to diverse human activities that have a profound impact on ecosystem functioning. These human activities are also ex pectedto alter interactions between aquatic hosts and their associated microbes. This can directly impact the host’s health and — given the importance and widespread occurrence of microbial symbiosis in aquatic systems — the ecosystem at large. In this review, we provide an overview of the importance of microbial symbionts for aquatic organisms, and we consider how the beneficial services provided by microbial symbionts can be affected by human activities. The scarcity of available studies that assess the functional consequences of human impacts on aquatic microbial symbioses shows that our knowledge on this topic is currently limited, making it difficult to draw general conclusions and predict future changes in microbial symbiont−host relationships in a changing world. To address this important knowledge gap, we provide an overview of ap proaches that can be used to assess the impact of human disturbances on the functioning of aquatic microbial symbioses. KEY WORDS: Host−symbiont interactions · Aquatic microbial symbioses · Mutualism · Anthropogenic disturbances © The authors 2021. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - #These authors contributed equally restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 114 Aquat Microb Ecol 87: 113–138, 2021 1. INTRODUCTION Fig. 1). This commonly used microbiome definition, however, is not fixed and often varies depending on A large fraction of ecological interactions within an the referenced source. There has been increased ecosystem are symbiotic, which can be defined as a research interest in the host-associated microbiota, phenomenon in which dissimilar organisms live facilitated through new DNA sequencing technolo- together (De Bary 1879). Although the term symbio- gies, which has revealed that many host organisms sis is mostly used in the context of mutualistic or com- support highly diverse communities of microbial mensalistic interactions between 2 species that live symbionts (Ley et al. 2008, White et al. 2016). In this in close contact for a substantial amount of time, it review, we discuss both specialized endosymbionts encompasses a whole spectrum of outcomes, includ- and the broader host-associated microbiota, as we ing parasitism. Furthermore, the outcome of a sym- expect some parallels in how they interact with the biosis between 2 species is not fixed, and both the host and how they are affected by environmental strength and direction (positive, neutral or negative) change. We only focus on microbial symbionts that of the interaction can change over time and/or shift provide — at least under some circumstances — a depending on the context (Daskin & Alford 2012). benefit to the host. Symbiosis can either be obligate, where one or both Most aquatic organisms start interacting with partners cannot survive without the other, or it can micro bial symbionts from their birth, and sometimes be facultative, with both partners able to survive even before (Bates et al. 2006, Nyholm 2020). Further- independently outside of the symbiosis. more, aquatic organisms acquire bacteria from the Microbial symbiosis refers to the phenomenon environment throughout their life cycle, making the where, in general, a larger organism (host) is colo- microbiota develop concomitantly with the host’s nized by smaller unicellular microorganisms (sym- chronological development. For several host organ- bionts). In aquatic environments, a wide diversity of isms, it has also been shown that they exert control eukaryote, bacterial and archaeal phyla engage in over the presence or abundance of specific symbionts, microbial symbiosis, either as host or symbiont often favouring beneficial symbiont strains (Rawls et (Grossart et al. 2013). Microbial symbionts can live as al. 2006, McFall-Ngai 2014, Tasiemski et al. 2015, endosymbionts within the cells or as specialized or- Stock et al. 2019a). These processes often en sure that gans of the host. However, many microbial symbionts the microbial community provides the necessary colonize the surface of epithelial tissues such as the functions throughout the host’s life cycle (Sampson & gut mucosa or are externally associated with the host, Mazmanian 2015, Dominguez-Bello et al. 2019). Mi- such as those growing in the phycosphere of micro- crobiota can be acquired from conspecifics through algae (Zoccarato & Grossart 2019). The assembly of maternal transmission or other forms of interactions, microorganisms found on a host is referred to as the or they can be acquired through colonization from the host-associated microbiota, and they form — in com- available pool of environmental microorganisms bination with their specific habitat and biological ac- (Funkhouser & Bordenstein 2013). The mode of trans- tivity — the micro biome (sensu Berg et al. 2020; mission is a key element in eco-evolutionary host− symbiont dynamics and is correlated AB C with symbiont function and degree of specialization (Macke et al. 2017b). Many (especially aquatic) organisms ob tain their microbiota through hori- zontal transmission, and the degree of exposure to environmental sources of microorganisms often plays a major role in determining microbiota assem- blies (Adair & Douglas 2017). Interme- diate modes, whereby symbionts from Fig. 1. Examples of aquatic host−symbiont associations. The host (largest organ- the parents are horizontally transmit- ism, grey) with its symbionts (unicellular eukaryotes, Archaea and Bacteria, ted to their offspring, have also been coloured). We define the symbionts as the microorganisms living in the host or ob served (Ebert 2013, Björk et al. externally associated with it. Well-studied examples of host− symbiont associa- 2019). Vertically transmitted symbi - tions (orange) include (A) Daphnia magna and its gut microbiota, (B) Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri and (C) Acropora spp. onts, which are transferred with high and the eukaryotic algae Symbiodinium spp. fidelity from the mother to the offspring Stock et al.: Human impact on aquatic symbioses 115 before birth, tend to resemble organelles, and their health. In Section 2 (‘Importance of the microbiome presence often has higher relevance for the host’s fit- for aquatic organisms’, summarized in Fig. 2A) we ness (Bright & Bulgheresi 2010, Fisher et al. 2017). In- provide an overview of the importance of microbial terestingly, aquatic host organisms seem to depend symbionts for coping with various challenges encoun- less on vertical transmission than terrestrial hosts tered by aquatic organisms. We focus on resource ac- (Russell 2019). quisition, physiological stress, predation, pathogens, It has become clear that, for many organisms, the parasites and host development. In Section 3 (‘Effects composition of their symbiont community has a major of anthropogenic disturbance on host− symbiont inter- influence on various physiological processes and, ul- actions’, summarized in Fig.