A Robust Species Tree for the Alphaproteobacteria

Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
Journal of Bacteriology (Impact Factor: 2.81). 08/2007; 189(13):4578-86. DOI: 10.1128/JB.00269-07
Source: PubMed


The branching order and coherence of the alphaproteobacterial orders have not been well established, and not all studies have
agreed that mitochondria arose from within the Rickettsiales. A species tree for 72 alphaproteobacteria was produced from a concatenation of alignments for 104 well-behaved protein families.
Coherence was upheld for four of the five orders with current standing that were represented here by more than one species.
However, the family Hyphomonadaceae was split from the other Rhodobacterales, forming an expanded group with Caulobacterales that also included Parvularcula. The three earliest-branching alphaproteobacterial orders were the Rickettsiales, followed by the Rhodospirillales and then the Sphingomonadales. The principal uncertainty is whether the expanded Caulobacterales group is more closely associated with the Rhodobacterales or the Rhizobiales. The mitochondrial branch was placed within the Rickettsiales as a sister to the combined Anaplasmataceae and Rickettsiaceae, all subtended by the Pelagibacter branch. Pelagibacter genes will serve as useful additions to the bacterial outgroup in future evolutionary studies of mitochondrial genes, including
those that have transferred to the eukaryotic nucleus.

Download full-text


Available from: Allan W Dickerman,
  • Source
    • "The best candidate source for this bacterium is also still α-proteobacteria (Gray 2012; Müller et al. 2012; Esposti 2014). This is primarily because most of the few remaining genes in mitochondrial genomes (mtDNAs) show α-proteobacterial affinity (Andersson et al. 2003; Esser et al. 2004; Fitzpatrick et al. 2006; Williams et al. 2007; Rodríguez-Ezpeleta and Embley 2012), as do 10-20% of the nuclear genes that encode 95-99% of the mitochondrial proteome (Szklarczyk and Huynen 2010; Thiergart et al. 2012; Gray 2015). Thus α-proteobacterial-like nuclear genes encoding mitochondrial proteins are presumed to have originated by transfer of genetic material from the mitochondrion to the nucleus (endosymbiotic gene transfer or EGT) (Timmis et al. 2004). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The most gene-rich and bacterial-like mitochondrial genomes (mtDNAs) known are those of Jakobida (Excavata). Of these, the most extreme example to date is the Andalucia godoyi mtDNA, including a cox15 gene encoding the respiratory enzyme heme A synthase (HAS), which is nuclear-encoded in nearly all other mitochondriate eukaryotes. Thus cox15 in eukaryotes appears to be a classic example of mitochondrion-to-nucleus (endosymbiotic) gene transfer, with A. godoyi uniquely retaining the ancestral state. However, our analyses reveal two highly distinct HAS types (encoded by cox15-1 and cox15-2 genes) and identify A. godoyi mitochondrial cox15-encoded HAS as type-1 and all other eukaryotic cox15-encoded HAS as type-2. Molecular phylogeny places the two HAS types in widely separated clades with eukaryotic type-2 HAS clustering with the bulk of alpha-proteobacteria (>670 sequences), while A. godoyi type-1 HAS clusters with an eclectic set of bacteria and archaea including two alpha-proteobacteria missing from the type-2 clade. This wide phylogenetic separation of the two HAS types is reinforced by unique features of their predicted protein structures. Meanwhile, RNA-sequencing and genomic analyses fail to detect either cox15 type in the nuclear genome of any jakobid including A. godoyi. This suggests that not only is cox15-1 a relatively recent acquisition unique to the Andalucia lineage, but the jakobid last common ancestor probably lacked both cox15 types. These results indicate that uptake of foreign genes by mtDNA is more taxonomically widespread than previously thought. They also caution against the assumption that all alpha-proteobacterial-like features of eukaryotes are ancient remnants of endosymbiosis.
    Molecular Biology and Evolution 09/2015; DOI:10.1093/molbev/msv201 · 9.11 Impact Factor
  • Source
    • "In a landmark study, Dumler et al. (2001) meticulously placed the majority of the species in these five genera into Neorickettsia, Wolbachia, Anaplasma, and Ehrlichia, with substantial revision of the latter two genera. Robust phylogeny estimations have supported the monophyly of the contemporary Anaplasmataceae, and its sister relationship with the Rickettsiaceae within Rickettsiales (Williams et al. 2007, Gillespie et al. 2012b, Driscoll et al. 2013). Neorickettsia spp. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Bacteria of the order Rickettsiales (Alphaproteobacteria) are gram-negative, small, rod-shaped, and coccoid, with all described species existing as obligate intracellular parasites of a wide range of eukaryotic organisms (Gillespie et al. 2012b). Before the DNA revolution, bacteria were assigned to Rickettsiales based primarily on chemical composition and morphology. Intraordinal classification employed a taxonomic system (i.e., generic characteristics) based on five major biological proper- ties: (1) human disease and geographic distribution, (2) natural vertebrate hosts and other animal vectors, (3) experimental infections and serology reactions and cross-reactions, (4) strain cultivation and stability, and (5) energy production and biosynthesis. This pioneering systematic work resulted in a Rickettsiales hierarchy of three families containing nine obligate and facultative intracellu- lar pathogenic genera: (1) Rickettsiaceae: genera Rickettsia, Coxiella, Rochalima, and Ehrlichia; (2) Bartonellaceae: genera Bartonella, Haemobartonella, Eperythrozoon, and Grahamella; and (3) Anaplasmataceae: genus Anaplasma. However, rickettsial classification has been substantially revised since the turn of the millennium, owing to the technological advances in molecular sequence genera- tion and the advent of several new fields of study, including molecular systematics, phylogenomics, and bioinformatics. Contemporary Rickettsiales taxonomy is radically different from the traditional system, with such tremendous changes as the reassignment of the Q-fever agent (Coxiella burnetii) to Gammaproteobacteria and the placement of the causative agents of several human diseases such as endocarditis, trench fever, and cat-scratch disease (Bartonella spp.) to the Order Rhizobiales.
    Practical Handbook of Microbiology, Third edited by Emmanuel Goldman, Lorrence H Green, 04/2015: chapter 31: pages 547-566; CRC Press., ISBN: 978-1-4665-8739-7
  • Source
    • "Please cite this article as: Pontieri, P., et al., Tellurium as a valuable tool for studying the prokaryotic origins of mitochondria, Gene (2015), http:// dx.doi.org/10.1016/j.gene.2015.01.060 endosymbiosis, either through the maintenance of hydrogenosomes, mitosomes or nuclear genes of mitochondrial origin (Gray et al., 2004; Embley and Martin, 2006), reasoning continues about the occasions of the founding endosymbiotic event (Embley and Martin, 2006; Koonin, 2010). Existing hypotheses, making use mitochondrial genome and proteome data, agree that the mitochondrial ancestor was most closely related to α-Proteobacteria (Andersson et al., 1998, 2003; Gray et al., 2001; Wu et al., 2004; Fitzpatrick et al., 2005; Esser et al., 2007; Williams et al., 2007; Ettema and Andersson, 2009). However, up to now the origin of the ancestral mitochondria within the α-Proteobacteria remains to be an unresolved question (Esser et al., 2004; Thrash et al., 2011). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Mitochondria are eukaryotic organelles which contain the own genetic material and evolved from free-living eubacteria, namely hydrogen-producing Alphaproteobacteria. Since 1965, biologists provided, by research at molecular level, evidence for the prokaryotic origins of mitochondria. However, determining the precise origins of mitochondria is challenging due to inherent difficulties in phylogenetically reconstructing ancient evolutionary events. The use of new tools to evidence the prokaryotic origin of mitochondria could be useful to gain an insight into the bacterial endosymbiotic event that resulted in the permanent acquisition of bacteria, from the ancestral cell, that through time were transformed into mitochondria. Electron microscopy has shown that both proteobacterial and yeast cells during their growth in the presence of increasing amount of tellurite resulted in dose-dependent blackening of the culture due to elemental tellurium (Te0) that formed large deposits either along the proteobacterial membrane or along the yeast cell wall and mitochondria. Since the mitochondrial inner membrane composition is similar to that of proteobacterial membrane, in the present work we evidenced the black tellurium deposits on both, cell wall and mitochondria of ρ+ and respiratory deficient ρ- mutants of yeast. A possible role of tellurite in studying the evolutionary origins of mitochondria will be discussed
    Gene 01/2015; 559(2). DOI:10.1016/j.gene.2015.01.060 · 2.14 Impact Factor
Show more