Symbiosis as a General Principle in Eukaryotic Evolution

Eukaryotes have evolved and diversified in the context of persistent colonization by non-pathogenic microorganisms. Various resident microorganisms provide a metabolic capability absent from the host, resulting in increased ecological amplitude and often evolutionary diversification of the host. Some microorganisms confer primary metabolic pathways, such as photosynthesis and cellulose degradation, and others expand the repertoire of secondary metabolism, including the synthesis of toxins that confer protection against natural enemies. A further route by which microorganisms affect host fitness arises from their modulation of the eukaryotic-signaling networks that regulate growth, development, behavior, and other functions. These effects are not necessarily based on interactions beneficial to the host, but can be a consequence of either eukaryotic utilization of microbial products as cues or host–microbial conflict. By these routes, eukaryote–microbial interactions play an integral role in the function and evolutionary diversification of eukaryotes.Eukaryotes do not live alone. They bear living cells of bacteria (Eubacteria and Archaea), and often eukaryotic microorganisms, on their surfaces and internally without any apparent ill effect. Furthermore, there is now persuasive evidence that all extant eukaryotes are derived from an association with intracellular bacteria within the Rickettsiales that evolved into mitochondria (Williams et al. 2007), with the implication that this propensity to form persistent associations has very ancient evolutionary roots. In this respect, the eukaryotes are different from the bacteria, among which only a subset associate with eukaryotes, specifically members of about 11 of an estimated 52 phyla of Eubacteria (Sachs et al. 2011) and a tiny minority of Archaea (Gill and Brinkman 2011).The current interest in the microbiota associated with eukaryotes stems from key technological advances for culture-independent analysis of microbial communities, especially high-throughput sequencing methods to identify and quantify microorganisms (Caporaso et al. 2011; Zaneveld et al. 2011). The Human Microbiome Project (commonfund.nih.gov), MetaHIT (metahit.eu), and other initiatives are yielding unprecedented information on the taxonomic diversity and functional capabilities of microorganisms associated with humans, other animals, and also plants, fungi, and unicellular eukaryotes (the protists), as well as abiotic habitats (Qin et al. 2010; Muegge et al. 2011; Human Microbiome Project 2012a; Lundberg et al. 2012; Bourne et al. 2013). Much of this research has focused on the Eubacteria, but eukaryotic members of the microbiota, especially the fungi, are increasingly being investigated (Iliev et al. 2012; Findley et al. 2013).Although driven by technological change, these culture-independent studies of the microbiota of humans and other eukaryotes are having profound consequences for our conceptual understanding. In particular, there is a growing appreciation that the germ theory of disease, which has played a crucial role in improving public health and food production through the 20th century, has also led to the widespread but erroneous belief that all microorganisms associated with animals and plants are pathogens. This outmoded perception is increasingly being replaced by the recognition that eukaryotes are chronically infected with benign and beneficial microorganisms, and that disease can result from disturbance to the composition or activities of the microbiota (McFall-Ngai et al. 2013; Stecher et al. 2013).This article reviews the pervasive impact of symbiosis with microorganisms on the traits of their eukaryotic hosts and the resultant consequences for the evolutionary history of eukaryotes. For the great majority of associations, the effects of symbiosis can be attributed to two types of interaction. The first interaction—“symbiosis as a source of novel capabilities”—is founded on metabolic or other traits possessed by the microbial partner but not the eukaryotic host. By gaining access to these capabilities, eukaryotes have repeatedly derived enhanced nutrition, defense against natural enemies, or other selectively important characteristics. The second interaction—“the symbiotic basis of health”—comprises the improved vigor and fitness that eukaryote hosts gain through microbial modulation of multiple traits, including growth rates, immune function, nutrient allocation, and behavior, even though the effects cannot be ascribed to specific microbial capabilities absent from the host. There is increasing evidence that the health benefits of symbiosis are commonly a consequence of microbial modulation of the signaling networks by which the growth and physiological function of eukaryote hosts are coordinated.This article comprises three sections: the two types of interaction are considered in turn, with the key patterns and processes illustrated by specific examples from a range of symbioses in animals, plants, and other eukaryotes; and the concluding comments address some key unanswered questions about symbiosis in eukaryotes. This article does not review the full diversity of associations made in this article on the general principles of symbiosis in eukaryotic evolution; interested readers are referred to Douglas (2010).