A place for host–microbe symbiosis in the comparative physiologist's toolbox

Abstract

Although scientists have long appreciated that metazoans evolved in a microbial world, we are just beginning to appreciate the profound impact that host-associated microbes have on diverse aspects of animal biology. The enormous growth in our understanding of hostmicrobe symbioses is rapidly expanding the study of animal physiology, both technically and conceptually. Microbes associate functionally with various body surfaces of their hosts, although most reside in the gastrointestinal tract. Gut microbes convert dietary and host-derived substrates to metabolites such as short-chain fatty acids, thereby providing energy and nutrients to the host. Bacterial metabolites incorporated into the host metabolome can activate receptors on a variety of cell types and, in doing so, alter host physiology (including metabolism, organ function, biological rhythms, neural activity and behavior). Given that host-microbe interactions affect diverse aspects of host physiology, it is likely that they influence animal ecology and, if they confer fitness benefits, the evolutionary trajectory of a species. Multiple variables -including sampling regime, environmental parameters, host metadata and analytical methods -can influence experimental outcomes in host-microbiome studies, making careful experimental design and execution crucial to ensure reproducible and informative studies in the laboratory and field. Integration of microbiomes into comparative physiology and ecophysiological investigations can reveal the potential impacts of the microbiota on physiological responses to changing environments, and is likely to bring valuable insights to the study of host-microbiome interactions among a broad range of metazoans, including humans.

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

“…Based on the conceptual framework above, of which we view as a further development of an existing component of the hologenome theory of evolution (Zilber-Rosenberg and Rosenberg, 2008; Rosenberg et al, 2009; Bordenstein and Theis, 2015), we identify three “signatures” for applying our hypothesis: diet, indirect life cycles, and seasonality (but see Kohl and Carey, 2016 for others). In doing so, we use examples from “model” and “non-model” animals across the animal kingdom with unique life-histories that may serve to answer sets of questions pertaining to evolutionary and ecological functions of the microbiome.…”

“…Thus, microbes can facilitate shifts in the permissible food sources from otherwise inaccessible energy sources (e.g., Hehemann et al, 2010), which may be a driving force in evolution of some groups (e.g., mammals; Ley et al, 2008; Alberdi et al, 2016). Microbial communities also respond to, and perhaps facilitate the host response to, prolonged periods of food deprivation (Kohl et al, 2014a) by providing the physiological toolkit that facilitates survival of the host (Turnbaugh et al, 2006, 2008, 2009; Mueller and Sachs, 2015; Kohl and Carey, 2016). In the context of the host-associated microbial repertoire, the sum of unique OTUs associated with the gut for each diet and feeding history along with the shared OTUs between them, enumerate H gut for an individual at a point in time.…”

“…Animals have diverse physiological and behavioral responses to the time of year that corresponds with seasonal changes, including periods elevating (e.g., reproduction and migration) and suppressing (e.g., hibernation and diapause) activity during life-history stages (Kohl and Carey, 2016). The associated microbes with a host that experience seasonal events change either in response to a new environment or in preparation for physiological shifts (Davenport et al, 2014; Kohl and Carey, 2016). One group that experiences an array of seasonally-driven ecological stressors that are also a well-studied system for animal-bacteria interactions in the marine environment (e.g., Lokmer and Wegner, 2015) are the bivalve mollusks.…”

“…Current theory and research on holobionts are now beginning to explicitly consider the variation in a natural environmental context, in part, because it is a necessary factor to understand the evolution of holobionts and hologenomes (Zilber-Rosenberg and Rosenberg, 2008; Theis et al, 2016). Studies of the host-associated microbial repertoire are useful in the effort to highlight the importance of microbes in host biology (e.g., physiology, development, immunology, behavior, population genetics; Jaenike, 2012; Eisthen and Theis, 2016; Kohl and Carey, 2016; Shropshire and Bordenstein, 2016) and ecology. Furthermore, this concept may aid in advancing our understanding of how these associations may have driven or directed the evolutionary trajectory of the holobiont, and their inheritable repertoire of symbiotic microbiota (van Opstal and Bordenstein, 2015; Gilbert, 2016).…”

Age‐related changes in the gut microbiota of the Chinese giant salamander (Andrias davidianus)

“…There are trillions of microorganisms living within multicellular organisms’ gastrointestinal (GI) tracts. These microbial communities play essential roles in the metabolism, physiology, ecology, and even evolution of their hosts (Colston, ; Colston, Noonan, & Jackson, ; Kohl & Carey, ; Zhu, Wu, Dai, Zhang, & Wei, ). A large amount of microorganismal research has centered on vertebrates (Ellis & McSweeney, ; Ley, Lozupone, Lozupone, Hamady, Knight, & Gordon, ); however, amphibians have been neglected and are potential model animals in gut microbial studies (Knutie, Wilkinson, Wilkinson, Kohl, & Rohr, ).…”