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Population Genetics and Phylogenetic Inference in Bacterial MOLECULAR PHYLOGENETICS AND EVOLUTION Molecular Phylogenetics and Evolution 34 (2005) 29–54 www.elsevier.com/locate/ympev Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation Pablo Vinuesaa,b,*, Claudia Silvaa, Dietrich Wernerb, Esperanza Martı´nez-Romeroa a Centro de Investigacio´n sobre Fijacio´n de Nitro´geno, Programa de Ecologı´a Molecular y Microbiana, UNAM, Av. Universidad S/N, Col. Chamilpa, AP 565-A, Cuernavaca CP 62210, Morelos, Me´xico b FB Biologie, FG fu¨r Zellbiologie und Angewandte Botanik, Philipps Universita¨t Marburg, Karl von Frisch Str, D-35032 Marburg, Germany Received 17 November 2003; revised 19 June 2004 Abstract A combination of population genetics and phylogenetic inference methods was used to delineate Bradyrhizobium species and to uncover the evolutionary forces acting at the population-species interface of this bacterial genus. Maximum-likelihood gene trees for atpD, glnII, recA, and nifH loci were estimated for diverse strains from all but one of the named Bradyrhizobium species, and three unnamed ‘‘genospecies,’’ including photosynthetic isolates. Topological congruence and split decomposition analyses of the three housekeeping loci are consistent with a model of frequent homologous recombination within but not across lineages, whereas strong evidence was found for the consistent lateral gene transfer across lineages of the symbiotic (auxiliary) nifH locus, which grouped strains according to their hosts and not by their species assignation. A well resolved Bayesian species phylogeny was estimated from partially congruent glnII + recA sequences, which is highly consistent with the actual taxonomic scheme of the genus. Population- level analyses of isolates from endemic Canarian genistoid legumes based on REP-PCR genomic fingerprints, allozyme and DNA polymorphism analyses revealed a non-clonal and slightly epidemic population structure for B. canariense isolates of Canarian and Moroccan origin, uncovered recombination and migration as significant evolutionary forces providing the species with internal cohesiveness, and demonstrated its significant genetic differentiation from B. japonicum, its sister species, despite their sympatry and partially overlapped ecological niches. This finding provides strong evidence for the existence of well delineated species in the bacterial world. The results and approaches used herein are discussed in the context of bacterial species concepts and the evo- lutionary ecology of (brady)rhizobia. Ó 2004 Elsevier Inc. All rights reserved. Keywords: Bayes factors; Canary islands; Coalescent simulations; Likelihood ratio test; Gene flow; Model selection; Neutrality tests; Partitioned models; Prokaryotes 1. Introduction cies, as broadly accepted for other asexual microbes and sexually reproducing macroscopic organisms The working hypothesis of this study is that speci- (Avise, 2000; Barraclough and Nee, 2001; Carbone ation in the bacterial world is the process that follows and Kohn, 2001; Cohan, 2001; Templeton, 1989). as gene flow diminishes and divergence increases The ‘‘phylophenetic’’ approach adopted by bacterial among populations, as the result of a variety of genet- taxonomists for species identification and delineation ic and ecological processes and historical contingen- (Rossello´-Mora and Amann, 2001; Stackebrandt et al., 2002; Vandamme et al., 1996) does not capture * Corresponding author. Fax: +52 777 3175581. this process adequately, as it relies on similarity crite- E-mail address: [email protected] (P. Vinuesa). ria (i.e., DNA homology values P60–70%, 63% rrs 1055-7903/$ - see front matter Ó 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2004.08.020 30 P. Vinuesa et al. / Molecular Phylogenetics and Evolution 34 (2005) 29–54 sequence divergence, and phenetic clustering), which 2002; Kurz and LaRue, 1975; Mesa et al., 2002; Saito cannot uncover the evolutionary forces that provide et al., 1998; So et al., 1994). species with internal cohesiveness, and shape their Despite this impressive diversity, only six species have population genetic structures. Based on the evidence been validly described so far: Bradyrhizobium japonicum accumulated during the last decade on the contrasting (Jordan, 1982), Bradyrhizobium elkanii (Kuykendall population genetic structures exhibited by different et al., 1992), Bradyrhizobium liaoningense (Xu et al., bacterial groups, which range from strictly clonal to 1995), Bradyrhizobium yuanmingense (Yao et al., 2002), essentially panmictic (Feil and Spratt, 2001; Istock Bradryrhizobium betae (Rivas et al., 2004), and Brady- et al., 1992; Maynard-Smith et al., 1993; Souza rhizobium canariense (Vinuesa et al., 2004). The first et al., 1992), the astronomic effective population sizes three species were isolated from soybean (Glycine max) of many free-living prokaryotes, and the extraordinary nodules. B. yuanmingense was isolated from Lespedeza diversity of prokaryotic lifestyles and ecological niches cuneata in China, B. betae from tumor-like root defor- they occupy (DeLong and Pace, 2001; Torsvik et al., mations of sugar beet (Beta vulgaris) in Northern Spain, 2002), we postulate that an interplay of diverse and B. canariense from diverse legume genera in the cohesion forces (such as recombination, migration, tribes Genisteae and Loteae growing naturally in the and selective sweeps) maintain species as recognizable Canary Islands, Morocco, Spain, the Americas and evolutionary lineages, and that these will differ among probably Australia (Jarabo-Lorenzo et al., 2003; Vinue- functional groups of prokaryotes and genomic regions sa et al., 2004). of individual strains. The phylogenetic relationships among these species This study was designed to gain insights into the evo- are poorly understood, mainly because only rrs se- lutionary processes operating at the population-species quences were analyzed in the reports describing them, interface of the bacterial genus Bradyrhizobium by using the exception being the description of B. canariense, a combination of population genetics and phylogenetic which was largely supported by the population genetics analyses (Lan and Reeves, 2001). This approach should and phylogenetic evidence presented herein. B. japoni- more properly capture the ecological and evolutionary cum isolates have been proposed to form at least two aspects of speciation in this cosmopolitan and diverse subgroups (I and Ia) based on DNA–DNA hybridiza- bacterial group, than that used in traditional rhizobial tion values (Hollis et al., 1981). Recently, ITS sequences taxonomy, and systematics (Sawada et al., 2003; Wil- have been obtained for a diverse set of bradyrhizobia, lems et al., 2001a,b). Based on 16S rRNA gene (rrs) se- including soybean isolates from the 17 described sero- quences, the genus Bradyrhizobium forms a clade in the types (van Berkum and Fuhrmann, 2000), isolates from a-2 subclass of the Proteobacteria along with oligo- diverse tropical and temperate legumes, including many trophic soil or aquatic bacteria such as Rhodopseudo- photosynthetic strains, as well as sequences of the gen- monas palustris, Rhodoplanes roseus, Nitrobacter era Afipia, Blastobacter, Nitrobacter,andRhodopseudo- winogradskyi, Blastobacter denitrificans, and the patho- monas (Tan et al., 2001; van Berkum and Eardly, gen Afipia spp. (Saito et al., 1998; Sawada et al., 2003; 2002; Willems et al., 2001a; Willems et al., 2003). These van Berkum and Eardly, 2002; Willems et al., 2001b). studies, coupled with extensive DNA–DNA hybridiza- Symbiotic Bradyrhizobium strains have been isolated tions led Willems et al. (2003) to propose seven new from the nodules of highly divergent legume tribes, both genospecies. However, ITS sequences do not properly from herbaceous and woody species, of tropical and resolve the evolutionary relationships among them (Vi- temperate origin, including aquatic legumes such as Aes- nuesa et al., 2004). Notable is the recent use of dnaK se- chynomene species, and the non-legume Parasponia quences for phylogenetic analyses of bradyrhizobia andersonii (Sprent, 2001). Bradyrhizobia have also been (Moulin et al., 2004), which corroborated rDNA-based found as endophytes of several rice species (Chaintreuil groupings, but did not resolve the relationships among et al., 2000; Tan et al., 2001). Probably the most out- them. standing aspect of the evolutionary ecology of bradyrhi- In this work, we generated a high number of atpD, zobia is that they cycle through highly contrasting glnII, recA, and nifH sequences of all the major Brady- lifestyles, as members of the communities of soil or rhizobium lineages (see Table S1, provided as supple- aquatic oligotrophic bacteria, as rhizospheric or endo- mentary material), and used maximum likelihood phytic bacteria, or as N2-fixing endosymbionts of di- (ML) and Bayesian frameworks to test diverse phyloge- verse host legume species. Bradyrhizobia are netic hypotheses, to infer a highly resolved species phy- metabolically diverse, some strains being capable of per- logeny for the genus, and to uncover the different forming denitrification or derepressing nitrogenase evolutionary histories of housekeeping and symbiotic activity under microaerobic free-living conditions, and loci. These analyses revealed that at least four Brady- yet others are photosynthetic or degrade xenobiotics rhizobium lineages nodulate diverse endemic Canarian such as 2,4-dichlorophenoxyacetate
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