Closely coupled evolutionary history of ecto‐ and endosymbionts from two distantly related animal phyla

Abstract

The level of integration between associated partners can range from ectosymbioses to extracellular and intracellular endosymbioses, and this range has been assumed to reflect a continuum from less intimate to evolutionarily highly stable associations. In this study, we examined the specificity and evolutionary history of marine symbioses in a group of closely related sulphur-oxidizing bacteria, called Candidatus Thiosymbion, that have established ecto-and endosymbioses with two distantly related animal phyla, Nematoda and Annelida. Intriguingly, in the ectosymbiotic associations of stilbonematine nematodes, we observed a high degree of congruence between symbiont and host phylogenies, based on their ribosomal RNA (rRNA) genes. In contrast, for the endosymbioses of gutless phallodriline annelids (oligochaetes), we found only a weak congruence between symbiont and host phylogenies, based on analyses of symbiont 16S rRNA genes and six host genetic markers. The much higher degree of congruence between nematodes and their ectosymbionts compared to those of annelids and their endosymbionts was confirmed by cophylogenetic analyses. These revealed 15 significant codivergence events between stilbonematine nematodes and their ectosymbionts, but only one event between gutless phallodrilines and their endosymbionts. Phylogenetic analyses of 16S rRNA gene sequences from 50 Cand. Thiosymbion species revealed seven well-supported clades that contained both stilbonematine ectosymbionts and phallodriline endosymbionts. This closely coupled evolutionary history of marine ecto-and endosymbionts suggests that switches between symbiotic lifestyles and between the two host phyla occurred multiple times during the evolution of the Cand. Thiosymbion clade, and highlights the remarkable flexibility of these symbiotic bacteria.

Co‐evolution of marine worms and their chemoautotrophic bacterial symbionts: unexpected host switches explained by ecological fitting?

“…The arguments that Zimmermann et al . () use to explain the flexibility of Candidatus Thiosymbion in its respective associations are in good agreement with the concept of ecological fitting. If all phylotypes have the same metabolic capacities and niche requirements, they can fulfil identical functions in different worms, as long as the host provides transport between oxidized and reduced sediment layers and no intricate adaptations are required during the shift from ectosymbiotic to endosymbiotic lifestyle.…”

“…Therefore, it was highly surprising that Zimmermann et al . () detected a high degree of congruence between the phylogenies of stilbonematines and their ectosymbionts (at least up to genus level) but only a single codivergence event between phallodrilines and their endosymbionts, which indicates that codiversification is restricted to the ectosymbiotic association. In addition, the monophyletic cluster of more than 50 phylotypes of Candidatus Thiosymbion included in their study comprised seven highly supported clades that contained both ectosymbionts and endosymbionts from the respective host groups.…”

“…In this issue of Molecular Ecology , Zimmermann et al . () investigated the evolutionary history of the symbiotic association between a monophyletic clade of sulphur‐oxidizing Gammaproteobacteria and two distantly related lineages of marine worms (nematodes and annelids). The study supports the surprising conclusion that partner fidelity does not necessarily increase with the intimacy of the association.…”

Specificity in diversity: single origin of a widespread ciliate-bacteria symbiosis

“…Codiversification between ectosymbiotic bacteria and motile eukaryotic hosts may seem surprising, as ectosymbionts are constantly exposed to their surrounding environment. However, recent studies have shown that the thiotrophic ectosymbionts of marine nematode worms [51] and the ectosymbionts of termite gut flagellates [52] have also cospeciated with their hosts, which highlights how codiversification and mechanisms for symbiont recognition and maintenance, previously assumed to be characteristic for endosymbioses, also occur in ectosymbioses.…”

“…Nonetheless, in Kentrophoros , both the host and symbiont clades remain specific and exclusive to each other, a pattern that has only been observed among thiotrophic symbioses in the flatworm Paracatenula [6] and the vesicomyid clams [55]. In other cases, a single symbiont clade may be associated with more than one host clade [51], or vice versa [56]. The apparently stable association between Kentrophoros and Ca .…”