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The Role of Symbioses in the Adaptation and Stress Responses of Marine Organisms MA12CH11_Apprill ARjats.cls November 16, 2019 11:33 Annual Review of Marine Science The Role of Symbioses in the Adaptation and Stress Responses of Marine Organisms Amy Apprill Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA; email: [email protected] Annu. Rev. Mar. Sci. 2020. 12:291–314 Keywords First published as a Review in Advance on holobiont, coevolution, ocean, coral reef, microorganism, climate July 5, 2019 The Annual Review of Marine Science is online at Abstract marine.annualreviews.org Ocean ecosystems are experiencing unprecedented rates of climate and an- https://doi.org/10.1146/annurev-marine-010419- thropogenic change, which can often initiate stress in marine organisms. Annu. Rev. Mar. Sci. 2020.12:291-314. Downloaded from www.annualreviews.org 010641 Symbioses, or associations between different organisms, are plentiful in the Copyright © 2020 by Annual Reviews. ocean and could play a signifcant role in facilitating organismal adaptations All rights reserved to stressful ocean conditions. This article reviews current knowledge about the role of symbiosis in marine organismal acclimation and adaptation. It dis- cusses stress and adaptations in symbioses from coral reef ecosystems, which are among the most affected environments in the ocean, including the rela- Access provided by Marine Biological Laboratory - Woods Hole Oceanographic Institution on 01/05/20. For personal use only. tionships between corals and microalgae, corals and bacteria, anemones and clownfsh, and cleaner fsh and client fsh. Despite the importance of this subject, knowledge of how marine organisms adapt to stress is still limited, and there are vast opportunities for research and technological development in this area. Attention to this subject will enhance our understanding of the capacity of symbioses to alleviate organismal stress in the oceans. 291 MA12CH11_Apprill ARjats.cls November 16, 2019 11:33 If you think about the coral that survived, those are the most robust genotypes. So that means what doesn’t kill you makes you stronger. Adaptation: —Ruth Gates (quoted in Kolbert 2016) a modifcation in the structure, physiology, immunology, 1. INTRODUCTION development, or Marine organisms are some of the most genetically, morphologically, metabolically, and behav- behavior of a species or iorally diverse life forms on Earth, and many of them also provide substantial services to humans population in response to changed conditions and to the ecosystems they inhabit (Costello et al. 2010, Duarte 2000). Marine organisms have de- veloped complex and innovative solutions for living within the dynamic ocean environment. For Symbiosis: persistent example, pelagic migrating animals are able to survive daily movements across steep gradients interactions between different organisms in temperature, pH, pressure, and prey or nutrient availability at different ocean depths. Adapta- tions have also played a role in the survival of sessile benthic organisms, which may experience diverse abiotic conditions, especially within intertidal and coastal habitats, but also need to fnd ways to obtain adequate nutrition, avoid predators, and/or prevent overgrowth of their benthic territory. Symbiosis has contributed to some of the innovative solutions needed to reside in these ocean environments and has provided opportunities for adaptations to occur over timescales much shorter than those of traditional mutation- and competition-driven adaptations. Marine organ- isms are currently facing unprecedented climate-based and other anthropogenically induced en- vironmental changes (Burrows et al. 2011, Doney et al. 2012, Hughes et al. 2018), and as these pressures persist and strengthen, symbiosis may become an even more important mechanism for driving organismal adaptation in the ocean. There are multiple defnitions of symbiosis. The term derives from the Greek sym-, meaning “together,” and bios, meaning “life,” and is generally used to describe dissimilar organisms living together (de Bary 1879). It can also refer to solely mutualistic associations (van Beneden 1873). Another interpretation considers the evolutionary aspect of relationships and refers to symbioses as long-term interactions that lead to novel capabilities (Douglas 1994). Not surprisingly, many scientists in the feld of symbiosis have their own defnitions for this term, but most investigators do agree that symbioses span a diverse range of organismal interactions, behaviors, and types of physical associations. The main types of symbiotic interactions are mutualism, commensalism, parasitism, and amen- salism (Figure 1a). Mutualism involves interactions that beneft both organisms; for example, clownfsh receive protection from anemones, and anemones in turn gain nutrients and protection from the clownfsh. Commensalism is benefcial to one or more organisms but has little or no Annu. Rev. Mar. Sci. 2020.12:291-314. Downloaded from www.annualreviews.org impact on the other partner. An example of this is barnacles, which settle on whales and thereby receive a substrate, but their presence does not affect the whale. Parasitism occurs when one or- ganism is harmed and another organism benefts, such as an isopod feeding on the tissues of fsh. Amensalism is a less examined type of symbiosis in which one organism is harmed but the other receives no beneft. An example of amensalism is a human-driven vessel that transits over a coral reef: The people on the ship gain no particular beneft from its location over the reef, but the ship Access provided by Marine Biological Laboratory - Woods Hole Oceanographic Institution on 01/05/20. For personal use only. produces sounds that mask the natural communication of reef organisms, which can negatively affect reef animals (Holles et al. 2013, Simpson et al. 2016). It may seem odd to include humans in an example of marine symbiosis; however, our species has a global and growing impact on ocean ecosystems and organisms (Halpern et al. 2008), and our activities have the potential to play a role in driving organismal evolution in the ocean. Symbioses vary in their level of dependency and physical association. In obligate symbioses (Figure 1b), the survival of one partner depends on the symbiosis. The relationship between corals 292 Apprill MA12CH11_Apprill ARjats.cls November 16, 2019 11:33 a Interaction types Mutualism Commensalism Parasitism Amensalism (+/+) (0/+) (–/+) (0/–) Anemone/clownfsh Whale/barnacle Fish/isopod Humans/ reef ecosystem b Dependency Obligate Facultative Coral/microalgae Hermit crab/anemone c Physical association Endosymbiosis Intracellular Extracellular Microalgae Bacteria Ectosymbiosis Constant contact Routine contact Bacteria on the skin of a grouper Cleaner fsh servicing a client host Annu. Rev. Mar. Sci. 2020.12:291-314. Downloaded from www.annualreviews.org Figure 1 Examples of the diverse types of interactions between organisms that constitute symbiosis, along with the Access provided by Marine Biological Laboratory - Woods Hole Oceanographic Institution on 01/05/20. For personal use only. various types of associated dependencies and physical associations. (a) The four types of symbiotic interactions, along with examples. A plus (+) indicates a beneft, a zero (0) indicates no beneft or harm, and aminus(−) indicates harm from the interaction. (b) The two types of symbiotic dependencies: obligate (necessary for the survival of at least one species) and facultative (in which both organisms can survive independent of the partnership). (c) Physical associations between symbiotic partners. In endosymbiosis, symbionts live either intracellularly within host cells (such as microalgae in corals) or extracellularly within the cavities surrounding host cells (such as some bacteria within corals). In ectosymbiosis, the partners may have consistent contact (such as bacteria on the surface of fsh) or less consistent but routine contact (such as a cleaner fsh interacting with a client host). www.annualreviews.org • Stress and Adaptation in Marine Symbioses 293 MA12CH11_Apprill ARjats.cls November 16, 2019 11:33 and their microalgae is an illustrative example of an obligate association: When corals lose their microalgal symbionts, a substantial source of their diet is gone, and this nutritional loss threatens their survival. By contrast, organisms within facultative host–symbiont associations are able to sur- Stress: a phenomenon b that is brought on by vive without their partner, as in the symbiosis between anemones and hermit crabs (Figure 1 ). biotic or abiotic factors The type of physical association between the organisms is also useful for describing symbiotic in- that cause a temporary teractions. Endosymbiosis refers to symbionts residing within the body of another organism, such or permanent as intracellular microalgae living within the gastrodermal cells of corals, or extracellular bacteria disruption of residing between the cells of the coral (Figure 1c). Ectosymbiosis describes symbionts residing homeostasis and can have negative ftness outside the body of the host. In this case, the symbiont may be in constant contact, as when an consequences if organism resides on the surface of a host (Figure 1c). In the marine environment, there are also ex- unmitigated amples of hosts and symbionts displaying routine external contact, such as the association between cleaner fsh and client fsh. Stress is a phenomenon that is brought on by biotic or abiotic factors that cause a tempo- rary
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