Evolutionary Stability in a 400-Million-Year-Old Heritable Facultative Mutualism

Abstract

Many eukaryotes interact with heritable endobacteria to satisfy diverse metabolic needs. Some of these interactions are facultative symbioses, in which one partner is not essential to the other. Facultative symbioses are expected to be transitional stages along an evolutionary trajectory toward obligate relationships. We tested this evolutionary theory prediction in Ca. Glomeribacter gigasporarum, nonessential endosymbionts of arbuscular mycorrhizal fungi (Glomeromycota). We found that heritable facultative mutualisms can be both ancient and evolutionarily stable. We detected significant patterns of codivergence between the partners that we would only expect in obligate associations. Using codiverging partner pairs and the fungal fossil record, we established that the Glomeromycota-Glomeribacter symbiosis is at least 400 million years old. Despite clear signs of codivergence, we determined that the Glomeribacter endobacteria engage in recombination and host switching, which display patterns indicating that the association is not evolving toward reciprocal dependence. We postulate that low frequency of recombination in heritable endosymbionts together with host switching stabilize facultative mutualisms over extended evolutionary times. K E Y W O R D S :Arbuscular mycorrhizal fungi, Ca. Glomeribacter gigasporarum, cospeciation, endosymbiosis, host switching, recombination.

Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi

“…Intracellular microbiome in arbuscular mycorrhizal fungi A Desirò et al history and, together with host switching, may have an important role in evolutionary stability of CaGg association with Glomeromycota (Mondo et al, 2012). Detecting evidence of recombination in a single gene of Mre sampled in the present study may suggest that Mre engage in more frequent recombination than CaGg.…”

“…Phylogenetic divergence patterns of the co-existing endobacteria The extensive phylogenetic analyses performed on the endobacteria thriving in the cytoplasm of five spore samples and their comparison with data from previous investigations (Bianciotto et al, 1996(Bianciotto et al, , 2000(Bianciotto et al, , 2003Mondo et al, 2012) confirmed that the 16S rRNA gene sequences of CaGg were relatively conserved, irrespective of the geographic origin of the fungal host. However, our careful analyses showed that the sequence similarity between CaGg from G. margarita MAFF520054 isolate and the already sequenced CaGg from G. margarita BEG34 was below the critical level of 97%.…”

“…Phenotypic consequences of CaGg removal from the host include important morphological changes as well as reduced proliferation of host presymbiotic hyphae. Yet, the host is not obligately dependent on the bacteria (Lumini et al, 2007;Mondo et al, 2012). These features suggest that Glomeribacter endobacteria are mutualistic associates of AMF (Lumini et al, 2007).…”

“…These features suggest that Glomeribacter endobacteria are mutualistic associates of AMF (Lumini et al, 2007). Comparisons of host and symbiont phylogenies indicate that, while CaGg is a heritable endosymbiont (Bianciotto et al, 2004), it also engages in recombination and host switching, which play an important role in stabilizing this 400-million-year-old association (Mondo et al, 2012). In contrast, information on the coccoid Mre is much more limited.…”

“…Two types of endosymbionts are known in AMF: (i) a rod-shaped, Gram-negative beta-proteobacterium (Bonfante et al, 1994), Candidatus Glomeribacter gigasporarum (CaGg), common in several species of the family Gigasporaceae (Bianciotto et al, 2003;Mondo et al, 2012), and (ii) a coccoid bacterium displaying a homogeneous Gram-positive-like wall structure (MacDonald et al, 1982;Scannerini and Bonfante, 1991), which represents a currently undescribed taxon of Mollicutesrelated endobacteria (Mre) with a wide distribution across Glomeromycota (Naumann et al, 2010).…”