Nature's microbiome: introduction

In recent years, it has become common knowledge that we, and the many organisms around us, are symbiotic creatures, harbouring large numbers of internal and external microbial residents. Research on symbiosis has progressed remarkably since the days of van Leeuwenhoek and de Bary, whose discoveries paved the way for over two centuries of fascinating work. Indeed, since their findings on bacteria in human mouths and algal-fungal partnerships that constitute lichens, we have discovered that microbial symbionts have shaped the make-up of the eukaryotic cell and that they continue to influence growth, development, energy metabolism, nutrition, digestion and defence of eukaryotes from across the globe (Wernegreen 2012; McFall-Ngai et al. 2013). It is now widely understood that microbial symbionts are important sources of innovation across eukaryotes, making symbiosis one of the hallmarks of eukaryotic biology. Historically, microscopy, analytical chemistry, antibiotic curing and a variety of other techniques were essential tools for the field, but recent innovations have propelled us into a golden age for symbiosis research. The identities and functions of both cultivable and noncultivable viruses, archaea, bacteria, protists and fungi can now be elucidated with genomic, transcriptomic or proteomic tools (Woyke et al. 2006; Warnecke et al. 2007; Engel et al. 2012; Kleiner et al. 2012; Sanders et al. 2013). Certain symbionts or hosts can be genetically modified, while some hosts can be manipulated via RNA interference, helping to understand the mechanisms behind symbiont colonization, persistence and functional contributions (Szeto et al. 1987; Dale et al. 2001; Radutoiu et al. 2003; Spiering et al. 2005). Furthermore, evolutionary histories of microbes and their hosts can be elucidated, revealing how commonly certain microbes have converged on lifestyles as symbionts and how they have spread across hosts over time (Zchori-Fein et al. 2001; Russell et al. 2003, 2009; Canback et al. 2004; Degnan et al. 2004; Pochon et al. 2004; Moran et al. 2008; Sachs et al. 2009; Mondo et al. 2012). Importantly, these molecular tools permit the study of symbiosis beyond model systems, enabling us to learn a good deal about uncultivable symbionts from hosts that are not amenable to laboratory or greenhouse rearing or to experimental manipulation. Perhaps no other field has been impacted by these new tools as much as human medicine, where it is now understood that nonpathogenic microbes play integral roles in health and immunity. The often-cited estimate of 100 times as many microbevs. human-encoded genes makes it clear that a good deal of novelty can be contributed by our microbiota (Backhed et al. 2005). But outside this field, nature’s microbiome—the communities of microbes colonizing host eukaryotes (Lederberg & McCray 2001)—has long been viewed as an important source of evolutionary novelty (Douglas 1989; Margulis 1996; Cavalier-Smith 2002). And innovations made through cutting-edge molecular research in many non-human organisms can tell us much about ourselves as well as life in the world around us. In this special issue of Molecular Ecology, we present 28 articles incorporating molecular and bioinformatics tools to dissect the intimate and prolonged associations that define symbioses. We have organized these studies into three sections, focused on (i) the composition of symbiotic communities and how this varies across hosts, tissues and development, and in response to environmental change (‘The Dynamic Microbiome’); (ii) the roles that microbes play for their hosts and the underlying mechanisms behind these functions (‘Microbiome Function’); and (iii) the nature and mechanisms of interactions between hosts and symbionts and between the co-inhabiting symbionts themselves (‘The Interactive Microbiome’). These articles highlight the state-of-the-art in microbiome research, with novel discoveries for well-developed models and for other budding systems beyond the human realm.