Microbiota mediated plasticity promotes thermal adaptation inNematostella vectensis

Abstract

At the current rate of climate change, it is unlikely that multicellular organisms will be able to adapt to changing environmental conditions through genetic recombination and natural selection alo. Thus, it is critical to understand alternative mechanisms that allow organisms to cope with rapid environmental changes. Here, we used the sea anemone Nematostella vectensis as model to investigate the microbiota as putative source of rapid adaptation. Living in estuarine ecosystems, highly variable aquatic environments, N. vectensis has evolved the capability of surviving in a wide range of temperatures and salinities. In a long-term experiment, we acclimated polyps of Nematostella to low, medium and high temperatures, in order to test the impact of microbiota-mediated plasticity on animal acclimation. Using the same animal clonal line, propagated from a single polyp, allowed us to eliminate effects of the host genotype. Interestingly, the higher thermal tolerance of animals acclimated to high temperature, could be transferred to non-acclimated animals through microbiota transplantation. In addition, offspring survival was highest from mothers acclimated to high temperature, indicating the transmission of thermal resistance to the next generation. Microbial community analyses of the F1 generation revealed the transmission of the acclimated microbiota to the next generation. These results indicate that microbiota plasticity can contribute to animal thermal acclimation and its transmission to the next generation may represent a rapid mechanism for thermal adaptation.

Genotype-environment interactions determine microbiota plasticity inNematostella vectensis

“…Rapidly dividing microbes are predicted to undergo adaptive evolution within weeks to months. Adaptation of the microbiota can occur via changes in absolute abundancies of specific members, acquisition of novel genes, mutation and/or horizontal gene transfer (Baldassarre, Ying, et al, 2021;Bang et al, 2018;Bay & Palumbi, 2015;Edwards, 2020;van Oppen et al, 2018). Here, we provide evidence for genotypespecific microbial plasticity, leading to genotype-specific restructuring of the microbial network in response to environmental stimuli.…”

“…Differences in prokaryotic community composition in different environments have been documented in many other marine invertebrates and are considered to reflect local acclimation (A Hernandez-Agreda et al, 2016;Glasl et al, 2019;Goldsmith et al, 2018;van Oppen et al, 2018). We have recently shown that the restructuring of microbial communities due to temperature acclimation is an important mechanism of host plasticity and adaptation in N. vectensis (Baldassarre, Ying, et al, 2021). The higher thermal tolerance of animals acclimated to high temperature could be transferred to non-acclimated animals through microbiota transplantation (Baldassarre, Ying, et al, 2021).…”

“…vectensis (Baldassarre, Ying, et al, 2021). The higher thermal tolerance of animals acclimated to high temperature could be transferred to non-acclimated animals through microbiota transplantation (Baldassarre, Ying, et al, 2021). In our study, high temperature conditions were particularly challenging for some genotypes native to north habitats, where they experience colder climate.…”

“…vectensis (Baldassarre, Ying, et al, 2021). The higher thermal tolerance of animals acclimated to high temperature could be transferred to non-acclimated animals through microbiota transplantation (Baldassarre, Ying, et al, 2021).…”