Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): a test of two symbiont-association models

Abstract

We reconstruct the phylogenetic relationships within the bacterial genus Pseudonocardia to evaluate two models explaining how and why Pseudonocardia bacteria colonize the microbial communities on the integument of fungus-gardening ant species (Attini, Formicidae). The traditional CoevolutionCodivergence model views the integument-colonizing Pseudonocardia as mutualistic microbes that are largely vertically transmitted between ant generations and that supply antibiotics that specifically suppress the garden pathogen Escovopsis. The more recent Acquisition model views Pseudonocardia as part of a larger integumental microbe community that frequently colonizes the ant integument from environmental sources (e.g., soil, plant material). Under this latter model, ant-associated Pseudonocardia may have diverse ecological roles on the ant integument (possibly ranging from pathogenic, to commensal, to mutualistic) and are not necessarily related to Escovopsis suppression. We test distinct predictions of these two models regarding the phylogenetic proximity of antassociated and environmental Pseudonocardia. We amassed 16S-rRNA gene sequence information for 87 attine-associated and 238 environmental Pseudonocardia, aligned the sequences with the help of RNA secondary structure modeling, and reconstructed phylogenetic relationships using a maximum-likelihood approach. We present 16S-rRNA secondary structure models of representative Pseudonocardia species to improve sequence alignments and identify sequencing errors. Our phylogenetic analyses reveal close affinities and even identical sequence matches between environmental Pseudonocardia and ant-associated Pseudonocardia, as well as nesting of Electronic supplementary material The online version of this article (doi:10.1007/s10482-010-9427-3) contains supplementary material, which is available to authorized users. environmental Pseudonocardia in subgroups that were previously thought to be specialized to associate only with attine ants. The great majority of ant associated Pseudonocardia are closely related to autotrophic Pseudonocardia and are placed in a large subgroup of Pseudonocardia that is known essentially only from cultured isolates (rather than cloned 16S sequences). The preponderance of the known ant-associated Pseudonocardia in this latter clade of culturable lineages may not necessarily reflect abundance of these Pseudonocardia types on the ants, but isolation biases when screening for Pseudonocardia (e.g., preferential isolation of autotrophic Pseudonocardia with minimum-nutrient media). The accumulated phylogenetic patterns and the possibility of isolation biases in previous work further erode support for the traditional Coevolution-Codivergence model and calls for continued revision of our understanding how and why Pseudonocardia colonize the microbial communities on the integument of fungus-gardening ant species. NIH Public Access

Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu, Hawaii populations

“…Taken together, this evidence suggests many key features related to the host E. scolopes (that is, local population structure; strong, selective environment; high symbiont population density) that might potentiate the evolution of local V. fischeri strains. Studies of other horizontal, 'binary' symbioses have argued that local host populations may have some influence on the local symbiont population structure and evolution (see, for example, Santos et al, 2003;Sicard et al, 2004;Cafaro et al, 2010;Maneesakorn et al, 2011), although other arguments also exist (for example, Martínez-Romero, 2009;Mueller et al, 2010), even within the squid/Vibrio symbiosis (Nishiguchi et al, 1998;Dunlap et al, 2007). For instance, using different phylogenetic markers and approaches, the latter two citations arrive at opposing conclusions concerning the evidence for parallel cladogenesis between species of squid and their light-organ symbionts.…”

Evolutionary transitions in bacterial symbiosis

“…Ancestral states for symbiotic lineage and evidence of mutualism breakdown were inferred by using parsimony on the available phylogenies (10,11,29,37,48,53,79,81,84,86,107,(112)(113)(114)(115)(116).…”

“…The most basal form of transmission is horizontal and likely occurs when bacteria are acquired from environmental pools (21,(80)(81)(82)(83)(84). In other cases of horizontal transmission, the symbiont taxa can be found in the environment (85,86), but most transmission likely occurs among hosts (16,60,61,87) with little contribution from environmental pools.…”

“…Two particularly dynamic examples of mutualism breakdown have been uncovered in symbionts of ants (84) and stinkbugs (79,107). In the case of the ants, the symbionts are antibiotic-producing Actinobacteria that live in cuticular crypts supported by specialized exocrine glands (19).…”

“…In the case of the ants, the symbionts are antibiotic-producing Actinobacteria that live in cuticular crypts supported by specialized exocrine glands (19). Lineages of these Actinobacteria have likely undergone multiple transitions between host-associated and environmental status based on the intermixing of symbiotic and environmental genotypes on a population-level phylogeny (84). Similarly, a phylogeny of the Burkholderia bug symbionts encompasses many environmental isolates, consistent with multiple transitions from symbiotic to environmental status (79).…”