Metaorganisms in extreme environments: do microbes play a role in organismal adaptation?

Abstract

From protists to humans, all animals and plants are inhabited by microbial organisms. There is an increasing appreciation that these resident microbes influence the fitness of their plant and animal hosts, ultimately forming a metaorganism consisting of a uni- or multicellular host and a community of associated microorganisms. Research on host-microbe interactions has become an emerging cross-disciplinary field. In both vertebrates and invertebrates a complex microbiome confers immunological, metabolic and behavioural benefits; conversely, its disturbance can contribute to the development of disease states. However, the molecular and cellular mechanisms controlling the interactions within a metaorganism are poorly understood and many key interactions between the associated organisms remain unknown. In this perspective article, we outline some of the issues in interspecies interactions and in particular address the question of how metaorganisms react and adapt to inputs from extreme environments such as deserts, the intertidal zone, oligothrophic seas, and hydrothermal vents.

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

“…Furthermore, the interaction between host and microbiota can potentially extend the metabolic capabilities of a holobiont in a way that augments its resilience to environmental changes (Berkelmans and van Oppen 2006;Gilbert et al 2010;Dittami et al 2016;Shapira 2016;Godoy et al 2018), or allow it to cross biotope boundaries (e.g. Woyke 2006) and colonize extreme environments (Bang et al 2018). Holobionts thus contribute to marine microbial diversity and possibly resilience in the context of global environmental changes (Troussellier et al 2017) and it is paramount to include the holobiont concept in predictive models that investigate the consequences of human impacts on the marine realm and its biogeochemical cycles.…”

Ecological specificity of the metagenome in a set of lower termite species supports contribution of the microbiome to adaptation of the host

“…The importance of microbes for the evolution of higher organisms is starting to be realized [1,2]. Metazoan evolution is not only driven by pathogenic microbes, as reflected by fast evolution of immune genes [3].…”

“…Metazoan evolution is not only driven by pathogenic microbes, as reflected by fast evolution of immune genes [3]. Rather, microbes often are facilitators of metabolic and environmental adaptations [2,4,5]. For instance, the gut microbial communities of wood-feeding roaches and termites facilitate thriving on a wood diet that is difficult to digest and poor in nitrogen.…”

“…For instance, the gut microbial communities of wood-feeding roaches and termites facilitate thriving on a wood diet that is difficult to digest and poor in nitrogen. Nitrogen fixation and the digestion of wood depend on the termite gut microbiome [2,6,7]. In lower termites, lignocellulose degradation was initially mainly attributed to unicellular eukaryotes (protists) in the gut [8].…”

Can the microbiome influence host evolutionary trajectories?

“…However, like other studies, we are only observing the endpoint of the host-microbiome evolutionary trajectory. Ultimately, understanding how microbiome alters the evolutionary trajectory in hosts is the critical missing link 122,[134][135][136][137][138][139][140][141] Bacterial diversity (family) Table 2 for summary of statistical tests. B) Evolved microbial diversity was only weakly correlated with host generations of selection (r = 0.24, p = 0.02).…”