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. 2021 Aug 19;19(8):e3001322.
doi: 10.1371/journal.pbio.3001322. eCollection 2021 Aug.

Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution

Matthieu Leray  1 , Laetitia G E Wilkins  2 , Amy Apprill  3 , Holly M Bik  4 , Friederike Clever  1   5 , Sean R Connolly  1 , Marina E De León  1   2 , J Emmett Duffy  6 , Leïla Ezzat  7 , Sarah Gignoux-Wolfsohn  8 , Edward Allen Herre  1 , Jonathan Z Kaye  9 , David I Kline  1 , Jordan G Kueneman  1 , Melissa K McCormick  8 , W Owen McMillan  1 , Aaron O'Dea  1   10 , Tiago J Pereira  4 , Jillian M Petersen  11 , Daniel F Petticord  1 , Mark E Torchin  1 , Rebecca Vega Thurber  12 , Elin Videvall  13   14 , William T Wcislo  1 , Benedict Yuen  11 , Jonathan A Eisen  2   15   16
Affiliations

Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution

Matthieu Leray et al. PLoS Biol. .

Abstract

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host's physiological capacities; however, the identity and functional role(s) of key members of the microbiome ("core microbiome") in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems' capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts' plastic and adaptive responses to environmental change requires (i) recognizing that individual host-microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Examples of marine natural experiments as observatories of host–microbe interactions.
Regionally focused, long-term, and taxonomically broad research programs will help fill key knowledge gaps about the nature of microbe functions and the dynamics of host–microbe interactions in changing oceans. We highlight areas of the world’s oceans where environmental gradients are well characterized, where the taxonomy and evolutionary history of the local host fauna and flora is already well established, where paleoecological studies can provide important historical context, where a long-term monitoring program is ongoing, and where there is significant research infrastructure. Long-term monitoring sites (white dots) include sites of the NSF’s LTER Network, the Smithsonian Institution’s MarineGEO network of partners, the MBON, the AIMS, and the ASSEMBLE. (1) NASA MODIS data; (2) Adapted from [93]; (3) Adapted from [73]; (4) Adapted from [74]; (5) Adapted from [94]; (6) Adapted from [95]. AIMS, Australian Institute of Marine Science; ASSEMBLE, Association of European Marine Biological Laboratories; LTER, Long-Term Ecological Research; MarineGEO, Marine Global Earth Observatory; MBON, Marine Biodiversity Observation Network.
Fig 2
Fig 2. Conceptual representation of the role of microbes in host acclimatization and adaptation.
Microbes can frequently adapt to environmental changes more rapidly than their host because of shorter generation times and higher standing genetic variation. Changes that occur at the levels of individual microbes and microbiomes can rapidly generate phenotypic plasticity in a broad range of host traits (i.e., one host genotype expresses multiple phenotypes induced by microbes). Microbially induced phenotypes may promote host adaptation if they become heritable traits. Within microbiomes, transient microbes (thin dashed circles) have limited effects on host phenotype. On the other hand, core microbes (thick dashed circles) that engage in prolonged relationships with hosts and potentially coevolve with hosts likely alter host phenotypes and promote host adaptation. Note that the time scale at which evolutionary changes occur varies widely between organisms, but adaptation is generally slower than acclimatization. Plain line: nonaltered interaction; dashed line: altered interaction; colors of microbes represent different microbial taxa.
Fig 3
Fig 3. The role of microbes in the host’s response to environmental changes is contingent upon their predominant mode of transmission.
Microbes that are present in the marine environment represent a vast pool of standing genetic variation. The majority of marine species with horizontal (e.g., lucinid clams and snapping shrimps) or mixed mode of symbiont acquisition (e.g., sponges) interact with a large number of microbes that they acquire during their lifetime. The ability to draw on this large evolutionary potential by switching microbes or gaining new genes potentially allows hosts to respond rapidly to environmental changes. At the other end of the spectrum, the few marine hosts with strictly vertically transmitted symbionts (e.g., flatworms) have less opportunity to exchange genes to rapidly adjust the symbiosis to changing conditions.
Fig 4
Fig 4. Methodological approach to leveraging a natural experiment, the Isthmus of Panama, for the long-term study of host–microbe ecology and evolution.
Present-day organisms physically separated by the Isthmus of Panama are adapted to the distinct environmental conditions of the productive TEP and the oligotrophic Caribbean. In the Gulf of Panama of the TEP, organisms experience some of the most drastic annual fluctuations in temperature, pH, oxygen, salinity, and nutrients, due to intense seasonal upwelling. Conversely, the nearby Gulf of Chiriquí of the TEP experiences weak to no upwelling due to trade winds being largely blocked by the Cordillera Central mountain range. Multidisciplinary and long-term research on hosts and associated microbes across these environmental spatiotemporal gradients, where decades of taxonomic, ecological, and evolutionary research can be leveraged, will help capture the dynamics of host–microbe interactions. TEP, Tropical Eastern Pacific.
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Grants and funding

Financial support for the workshop was provided by grant GBMF5603 (https://doi.org/10.37807/GBMF5603) from the Gordon and Betty Moore Foundation (W.T. Wcislo, J.A. Eisen, co-PIs), and additional funding from the Smithsonian Tropical Research Institute and the Office of the Provost of the Smithsonian Institution (W.T. Wcislo, J.P. Meganigal, and R.C. Fleischer, co-PIs). JP was supported by a WWTF VRG Grant and the ERC Starting Grant 'EvoLucin'. LGEW has received funding from the European Union’s Framework Programme for Research and Innovation Horizon 2020 (2014-2020) under the Marie Sklodowska-Curie Grant Agreement No. 101025649. AO was supported by the Sistema Nacional de Investigadores (SENACYT, Panamá). A. Apprill was supported by NSF award OCE-1938147. D.I. Kline, M. Leray, S.R. Connolly, and M.E. Torchin were supported by a Rohr Family Foundation grant for the Rohr Reef Resilience Project, for which this is contribution #2. This is contribution #85 from the Smithsonian’s MarineGEO and Tennenbaum Marine Observatories Network. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.