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Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis [1]

['Laura Baldassarre', 'Institut Für Zoologie Und Organismische Interaktionen', 'Heinrich-Heine Universität Düsseldorf', 'Düsseldorf', 'Istituto Nazionale Di Oceanografia E Di Geofisica Sperimentale Ogs', 'Sezione Di Oceanografia', 'Trieste', 'Adam M. Reitzel', 'Department Of Biological Sciences', 'University Of North Carolina At Charlotte']

Date: 2023-01

Most multicellular organisms harbor microbial colonizers that provide various benefits to their hosts. Although these microbial communities may be host species- or even genotype-specific, the associated bacterial communities can respond plastically to environmental changes. In this study, we estimated the relative contribution of environment and host genotype to bacterial community composition in Nematostella vectensis, an estuarine cnidarian. We sampled N. vectensis polyps from 5 different populations along a north–south gradient on the Atlantic coast of the United States and Canada. In addition, we sampled 3 populations at 3 different times of the year. While half of the polyps were immediately analyzed for their bacterial composition by 16S rRNA gene sequencing, the remaining polyps were cultured under laboratory conditions for 1 month. Bacterial community comparison analyses revealed that laboratory maintenance reduced bacterial diversity by 4-fold, but maintained a population-specific bacterial colonization. Interestingly, the differences between bacterial communities correlated strongly with seasonal variations, especially with ambient water temperature. To decipher the contribution of both ambient temperature and host genotype to bacterial colonization, we generated 12 clonal lines from 6 different populations in order to maintain each genotype at 3 different temperatures for 3 months. The bacterial community composition of the same N. vectensis clone differed greatly between the 3 different temperatures, highlighting the contribution of ambient temperature to bacterial community composition. To a lesser extent, bacterial community composition varied between different genotypes under identical conditions, indicating the influence of host genotype. In addition, we identified a significant genotype x environment interaction determining microbiota plasticity in N. vectensis. From our results we can conclude that N. vectensis-associated bacterial communities respond plastically to changes in ambient temperature, with the association of different bacterial taxa depending in part on the host genotype. Future research will reveal how this genotype-specific microbiota plasticity affects the ability to cope with changing environmental conditions.

Funding: This work was supported by the Human Frontier Science Program ( https://www.hfsp.org/ ) (Young Investigators' Grant RGY0079/2016) to AR and SF and the Deutsche Forschungsgemeinschaft ( https://www.dfg.de/ ), CRC grant 1182 “Origin and Function of Metaorganisms” (Project B1) to SF. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Introduction

Most multicellular organisms live in association with microbial symbionts [1,2]. It has been widely demonstrated that these symbionts provide various benefits for the survival and persistence of their hosts [3–5]. The quality and quantity of associated microbial species is characteristic for host species [6–8], genotype [9,10], biogeography [11–13], life stage [14–17], diet [18–20], and environmental conditions [12,13,21,22]. Starting from these evidences, many studies demonstrated that the host plays an active role in shaping its symbiont microbiota [7,23–26]. In addition to the effects of the host and the environment, the interaction between these 2 factors is also discussed as a potential factor influencing the plasticity of the microbiota [27].

Nematostella vectensis is a small, burrowing estuarine sea anemone found in tidally restricted salt marsh pools. The distribution of this species extends over the Atlantic and Pacific coasts of North America and the southeast coast of England [28] and its range encompasses large latitudinal variation in temperature and salinity [29]. N. vectensis’ wide environmental tolerance and broad geographic distribution [28,30], combined with the availability of a genome sequence [31] make it an exceptional organism for exploring adaptations to variable environments. N. vectensis has separated sexes and it is able to reproduce both sexually through external fertilization [30,32,33] and asexually through transverse fission [28]. Although a free-swimming larval stage is present, this species is considered to have overall pretty limited dispersal abilities [34]. Seasonal population fluctuations in density may lead to frequent bottlenecks, and when gene flow between subpopulations is restricted by physical barriers, such fluctuations could result in conspicuous genetic structuring between locations over short geographic distances [34,35]. Completely or largely clonal populations exist all through the distribution range of N. vectensis [28,34,36]; however, microsatellite and SNP markers indicated an extensive intraspecific genetic diversity and genetic structuring between populations in their native range along the Atlantic coast of North America [37,38].

Within a single estuary, N. vectensis occupies tidal streams that flush with each tide or, isolated still-water high-marsh pools, that can differ substantially in a set of ecological variables including temperature and salinity [39,40]. Previous works showed that different N. vectensis genotypes from same natural pools within a single estuary have significantly different tolerances to oxidative stress [39] and that individuals from different field populations respond differently to same thermal conditions during lab culturing [41].

An initial categorization of the N. vectensis microbiota has shown that individuals from different field pools of the North American Atlantic coast have significantly different microbiota and that these differences follow a north–south gradient [12]. The different ecological conditions that distinguish these pools from each other and the genetic structuring of N. vectensis populations led us to hypothesize that the microbiota is a subject to local selection. In particular, locally adapted host genotypes may associate with symbionts that provide advantages at the specific ecological conditions of each native pool. Recently, we have shown that genetically identical animals differentiate their microbiome composition in response to a change in environmental temperature. By transplanting the adapted microbiome onto non-adapted animals, we demonstrated that the observed microbiome plasticity leads to increased tolerance of the animals to thermal stress [21]. However, the influence of the host genotype on the plasticity of the microbiome and thus on the ability to cope with changing environmental conditions remained unclear.

In this study, we analyzed the microbiota composition of polyps from different populations directly after sampling and after 1 month of laboratory maintenance. We first investigated which factors among ambient temperature, salinity, season, and geographic location, contribute to microbiota differentiation. The results of these analyses show that the composition of the microbiota changes with both season and geographic location, and that these differences persist under laboratory conditions. Consistent with previous laboratory observations [12], our field data confirmed that temperature, over salinity, is correlating the most with differences in bacterial community compositions. Starting from these evidences, we investigated the influence of ambient temperature on the microbiota plasticity of 12 individual genotypes derived from 6 different populations. We found that after 3 months of laboratory culture, temperature was the factor most driving microbiota differentiation, although differences according to genotype were also detectable. In addition, we demonstrated that microbiota plasticity in relation to temperature is genotype-specific, suggesting that microbiota plasticity is also influenced by interactions between genotype and temperature.

With this study, we have taken an important step toward understanding the contribution of both local environmental conditions and host genotype in shaping the microbiota. Furthermore, we have shown that although microbial community dynamics are plastic, each genotype is associated with a microbiota that exhibits genotype-specific flexibility. These results suggest that local populations of the same species may have different abilities to adapt to environmental changes through microbiota-mediated plasticity.

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001726

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