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New rRNA gene-based phylogenies of the Alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability.

ABSTRACT: Bacteria in the class Alphaproteobacteria have a wide variety of lifestyles and physiologies. They include pathogens of humans and livestock, agriculturally valuable strains, and several highly abundant marine groups. The ancestor of mitochondria also originated in this clade. Despite significant effort to investigate the phylogeny of the Alphaproteobacteria with a variety of methods, there remains considerable disparity in the placement of several groups. Recent emphasis on phylogenies derived from multiple protein-coding genes remains contentious due to disagreement over appropriate gene selection and the potential influences of systematic error. We revisited previous investigations in this area using concatenated alignments of the small and large subunit (SSU and LSU) rRNA genes, as we show here that these loci have much lower GC bias than whole genomes. This approach has allowed us to update the canonical 16S rRNA gene tree of the Alphaproteobacteria with additional important taxa that were not previously included, and with added resolution provided by concatenating the SSU and LSU genes. We investigated the topological stability of the Alphaproteobacteria by varying alignment methods, rate models, taxon selection and RY-recoding to circumvent GC content bias. We also introduce RYMK-recoding and show that it avoids some of the information loss in RY-recoding. We demonstrate that the topology of the Alphaproteobacteria is sensitive to inclusion of several groups of taxa, but it is less affected by the choice of alignment and rate methods. The majority of topologies and comparative results from Approximately Unbiased tests provide support for positioning the Rickettsiales and the mitochondrial branch within a clade. This composite clade is a sister group to the abundant marine SAR11 clade (Pelagibacterales). Furthermore, we add support for taxonomic assignment of several recently sequenced taxa. Accordingly, we propose three subclasses within the Alphaproteobacteria: the Caulobacteridae, the Rickettsidae, and the Magnetococcidae.

SUBMITTER: Ferla MP

PROVIDER: S-EPMC3859672 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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New rRNA gene-based phylogenies of the Alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability.

Ferla Matteo P MP Thrash J Cameron JC Giovannoni Stephen J SJ Patrick Wayne M WM

PloS one 20131211 12

Bacteria in the class Alphaproteobacteria have a wide variety of lifestyles and physiologies. They include pathogens of humans and livestock, agriculturally valuable strains, and several highly abundant marine groups. The ancestor of mitochondria also originated in this clade. Despite significant effort to investigate the phylogeny of the Alphaproteobacteria with a variety of methods, there remains considerable disparity in the placement of several groups. Recent emphasis on phylogenies derived ...[more]

PMID: 24349502

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Project description:BackgroundThe 16S rRNA gene is used extensively in bacterial phylogenetics, in species delineation, and now widely in microbiome studies. However, the gene suffers from intragenomic heterogeneity, and reports of recombination and an unreliable phylogenetic signal are accumulating. Here, we compare core gene phylogenies to phylogenies constructed using core gene concatenations to estimate the strength of signal for the 16S rRNA gene, its hypervariable regions, and all core genes at the intra- and inter-genus levels. Specifically, we perform four intra-genus analyses (Clostridium, n = 65; Legionella, n = 47; Staphylococcus, n = 36; and Campylobacter, n = 17) and one inter-genus analysis [41 core genera of the human gut microbiome (31 families, 17 orders, and 12 classes), n = 82].ResultsAt both taxonomic levels, the 16S rRNA gene was recombinant and subject to horizontal gene transfer. At the intra-genus level, the gene showed one of the lowest levels of concordance with the core genome phylogeny (50.7% average). Concordance for hypervariable regions was lower still, with entropy masking providing little to no benefit. A major factor influencing concordance was SNP count, which showed a positive logarithmic association. Using this relationship, we determined that 690 ± 110 SNPs were required for 80% concordance (average 16S rRNA gene SNP count was 254). We also found a wide range in 16S-23S-5S rRNA operon copy number among genomes (1-27). At the inter-genus level, concordance for the whole 16S rRNA gene was markedly higher (73.8% - 10th out of 49 loci); however, the most concordant hypervariable regions (V4, V3-V4, and V1-V2) ranked in the third quartile (62.5 to 60.0%).ConclusionsRamifications of a poor phylogenetic performance for the 16S rRNA gene are far reaching. For example, in addition to incorrect species/strain delineation and phylogenetic inference, it has the potential to confound community diversity metrics if phylogenetic information is incorporated - for example, with popular approaches such as Faith's phylogenetic diversity and UniFrac. Our results highlight the problematic nature of these approaches and their use (along with entropy masking) is discouraged. Lastly, the wide range in 16S rRNA gene copy number among genomes also has a strong potential to confound diversity metrics. Video Abstract.

Project description:Background and aimsHieracium subgenus Hieracium is one of the taxonomically most intricate groups of vascular plants, due to polyploidy and a diversity of breeeding systems (sexuality vs. apomixis). The aim of the present study was to analyse nuclear genome size in a phylogenetic framework and to assess relationships between genome size and ploidy, breeding system and selected ecogeographic features.MethodsHoloploid and monoploid genome sizes (C- and Cx-values) of 215 cultivated plants from 89 field populations of 42 so-called 'basic' Hieracium species were determined using propidium iodide flow cytometry. Chromosome counts were available for all analysed plants, and all plants were tested experimentally for their mode of reproduction (sexuality vs. apomixis). For constructing molecular phylogenetic trees, the external transcribed spacer region of nuclear ribosomal DNA was used.Key resultsThe mean 2C values differed up to 2.37-fold among different species (from 7.03 pg in diploid to 16.67 in tetraploid accessions). The 1Cx values varied 1.22-fold (between 3.51 and 4.34 pg). Variation in 1Cx values between conspecific (species in a broad sense) accessions ranged from 0.24% to 7.2%. Little variation (not exceeding the approximate measurement inaccurracy threshold of 3.5%) was found in 33 species, whereas variation higher than 3.5% was detected in seven species. Most of the latter may have a polytopic origin. Mean 1Cx values of the three cytotypes (2n, 3n and 4n) differed significantly (average of 3.93 pg in diploids, 3.82 pg in triploids and 3.78 pg in tetraploids) indicating downsizing of genomes in polyploids. The pattern of genome size variation correlated well with two major phylogenetic clades which were composed of species with western or eastern European origin. The monoploid genome size in the 'western' species was significantly lower than in the 'eastern' ones. Correlation of genome size with latitude, altitude and selected ecological characters (light and temperature) was not significant. A longitudinal component was only apparent for the whole data set, but absent within the major lineages.ConclusionsPhylogeny was the most important factor explaining the pattern of genome size variation in Hieracium sensu stricto, species of western European origin having significantly lower genome size in comparison with those of eastern European origin. Any correlation with ecogeographic variables, including longitude, was outweighed by the divergence of the genus into two major phylogenetic lineages.

Dataset Information

New rRNA gene-based phylogenies of the Alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability.

Publications

New rRNA gene-based phylogenies of the Alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability.

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