Evolutionary transitions in bacterial symbiosis

Abstract

Diverse bacterial lineages form beneficial infections with eukaryotic hosts. The origins, evolution, and breakdown of these mutualisms represent important evolutionary transitions. To examine these key events, we synthesize data from diverse interactions between bacteria and eukaryote hosts. Five evolutionary transitions are investigated, including the origins of bacterial associations with eukaryotes, the origins and subsequent stable maintenance of bacterial mutualism with hosts, the capture of beneficial symbionts via the evolution of strict vertical transmission within host lineages, and the evolutionary breakdown of bacterial mutualism. Each of these transitions has occurred many times in the history of bacterial-eukaryote symbiosis. We investigate these evolutionary events across the bacterial domain and also among a focal set of well studied bacterial mutualist lineages. Subsequently, we generate a framework for examining evolutionary transitions in bacterial symbiosis and test hypotheses about the selective, ecological, and genomic forces that shape these events.

Fig. 1.

Inferred evolutionary history of bacterial host association. Ancestral states are inferred on a domain-level bacterial phylogeny modified from a previous study (9). Fig. S1 and Table S1 provide taxon labels. The tree is a maximum likelihood reconstruction of a concatenated set of 31 single-copy genes from 350 bacterial species chosen to optimize phylogenetic sampling. Phyla and proteobacterial classes are labeled with their full names (e.g., Gammaproteobacteria; Firmicutes) or single-letter abbreviations (a, Acidobacteria; d, Defferribacteres; q, Aquificae; e, Elusimicrobia; v, Verrucomicrobia; p, Planctomycetes). Branch colors represent host-associated traits on the tips of the tree and inferred states on ancestral nodes (black, environmental; blue, commensal; green, mutualist; red, parasite). Host association traits were obtained from a prior review (4). We inferred a minimum of 42 origins of host-association (labeled 1–42). Origins at five nodes had equivocal parsimony reconstructions, noted with asterisks. Equivocal ancestral states are represented by blended branch colors (brown, environmental or parasite; purple, parasite or commensal; yellow, parasite or mutualist). Additional origins are equally parsimonious at these nodes and provide an upper bound for global origins at 52. (Adapted from ref. .)

Fig. 2.

Symbiont housing structures and their potential to promote spatial structure. (A) Host Ascidian Diplosoma spp. and symbiont Prochloron spp. unstructured in host cloacal cavity (Reprinted from ref. 28). (B) Host hydrothermal tubeworm Riftia pachyptila with symbiont Endoriftia persephone (s, red) unstructured in host trophosome (Reprinted from ref. 21). (C) Antenna of host beewolf Philanthus triangulum with symbiont Streptomyces (ws, red) housed in structured serial antennomere reservoirs (cross-section above; longitudinal section below) (Reprinted from ref. 23). (D). Four-chambered midgut of host stinkbug Dimorphopterus pallipes with symbiont Burkholderia spp. (s) housed in structured crypts of fourth midgut section (m4) (Reprinted from ref. 79). (E) Juvenile squid host Euprymna scolopes during colonization by symbiont V. fischeri, housed in structured deep crypts (dc; Adapted from ref. .) (F) Host mouse small intestine and symbiont B. thetaiotaomicron (blue capsules) in structured crypts of Lieberkuhn (c) based with Paneth cells (p) (Adapted from ref. 24). (G) Dorsal cross-section of host ant Cyphomyrmex longiscapus with Actinomyces symbionts (s) housed in structured crypts (Reprinted from ref. 19). (H) Host legume Lotus strigosus with symbiont Bradyrhizobium japonicum structured in four numbered nodules (photo by J. L. Sachs).

Fig. 3.

Path diagram of evolutionary transitions among bacterial host-association types. Transitions among four bacterial host-association types inferred in the tree by Wu and colleagues (9) using lifestyle data from Toft and Anderson (4). Com., commensal; Env., environmental; Mut., mutualist; Par., parasite. Thirteen transitions were undetermined on the tree as a result of ambiguity. There were zero transitions between mutualism and commensalism and zero transitions from commensalism to parasitism. Arrow sizes are scaled to the number of transitions between host-association types.