The Hologenome Across Environments and the Implications of a Host-Associated Microbial Repertoire

Tyler J. Carrier, Adam M. Reitzel

Our understanding of the diverse interactions between hosts and microbes has grown profoundly over the past two decades and, as a product, has revolutionized our knowledge of the life sciences. Through primarily laboratory experiments, the current framework for holobionts and their respective hologenomes aims to decipher the underpinnings and implications of symbioses between host and microbiome. However, the laboratory setting restricts the full spectrum of host-associated symbionts as compared to those found in nature; thus, limiting the potential for a holistic interpretation of the functional roles the microbiome plays in host biology. When holobionts are studied in nature, associated microbial communities vary considerably between conditions, resulting in more microbial associates as part of the "hologenome" across environments than in either environment alone. We review and synthesize empirical evidence suggesting that hosts may associate with a larger microbial network that, in part, corresponds to experiencing diverse environmental conditions. To conceptualize the interactions between host and microbiome in an ecological context, we suggest the "host-associated microbial repertoire," which is the sum of microbial species a host may associate with over the course of its life-history under all encountered environmental circumstances. Furthermore, using examples from both terrestrial and marine ecosystems, we discuss how this concept may be used as a framework to compare the ability of the holobiont to acclimate and adapt to environmental variation, and propose three "signatures" of the concept.