Here come the commensals

Abstract

Metagenomic approaches to understanding microbial symbiont communities, the microbiome, have provided an unprecedented window into the diversity of microbial organisms associated with virtually all eukaryotic hosts. However, our ignorance of what these symbionts do has been illuminated as well. Nowhere is the contrast between what we know, and what we do not know, more starkly realized than in the Kingdom Fungi with descriptions of less than 5% of the estimated 1.5 to 5 million taxa (Blackwell, 2011). While there is delight in discovery, and fortitude in the face of the cryptic nature of fungal symbioses, understanding the diversity of ecologi-cal functions for fungal symbionts remains a formidable challenge. Here, I use endophytic fungi to draw attention to the particular co-nundrum of commensal symbionts, symbionts that seem to do lit-tle but likely make up most of the microbial communities occupying plant and animal hosts. Endophytic fungi are those symbionts liv-ing within healthy living tissues of plants (Wilson, 1995) and thus, in terms of their interactions with the host, are best considered commensals. H. Anton de Bary in 1878 put commensals squarely in the middle of the continuum of symbioses between benefi cial mu-tualists and detrimental parasites because commensals have few ap-parent direct eff ects on their hosts (translation by Oulhen et al., 2016). Others have argued against typecasting commensal symbio-ses as those in which nothing happens (Hirsh and Fujishige, 2008) or those for which we do not know what happens (Zapalski, 2011). Here, I advocate for the perspective that the commensal symbi-otic habit is critical to study because commensalism enables the evolution and maintenance of tremendous diversity in ecological functions. THEORY AND CONCEPT Th e pervasive assumption that microbiome symbionts, including endophytic fungi, must benefi t the host echoes the " balance of na-ture " perspectives found in early theoretical and conceptual models for parasites and for microbiomes. For parasites, virulence was thought maladaptive because the host on which the microbe de-pends is damaged and evolution toward low virulence states was predicted (reviewed by Ewald, 1983). For the human microbiome, Henderson and Wilson (1998 , p. 1680) posited that diverse micro-bial communities " evolved cytokine-modulating molecules to live in harmony with host mucosal surfaces " and envisioned the micro-biome as a communistic collective. In contrast, modern theory pre-dicts that competition for host resources among multiple infecting symbionts should drive the evolution of greater virulence toward the host (reviewed by Alizon et al., 2013). Limits to virulence arise from a trade-off between parasite reproduction and parasite-induced host mortality (Anderson and May, 1982). Still, with the explosion of research on the microbiome, the concept that the " holobiont " (host plus microbes) evolves as a superorganism has been strongly forwarded (Bordenstein and Th eis, 2015) and ac-tively debated (Moran and Sloan, 2015). One way out of this con-ceptual mess may come from results that suggest a very dynamic nature of microbiome communities (Burns et al., 2016) with rela-tively few taxa comprising a " core microbiome " (Douglas and Werren, 2016). Employing evolutionary models that bring in " third party " interactions, we might then predict that the ever-changing landscape of microbial symbionts drives the evolution of traits such as antagonism against microbial competitors. Further, if ecological outcomes are conditional on population history and the identity of interacting species, as seems to be the case for endophytic fungi (Busby et al., 2016b), tremendous variation in traits that aff ect these interactions can be maintained species-wide (Bronstein, 1994 ; Gomulkiewicz et al., 2003). For now, we might best assume that most symbiotic species of the microbiome muddle along, pulled in diff erent directions by the ever-changing ecological context set up by the nature of the commensal habit. Occasionally, but impor-tantly, commensals " escape " and evolve more extreme symbiotic modes toward the host—mutualism and parasitism. WHY COMMENSAL SYMBIONTS ARE INTERESTING TO STUDY