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Battistuzzi2009chap07.Pdf Eubacteria Fabia U. Battistuzzia,b,* and S. Blair Hedgesa shown increasing support for lower-level phylogenetic Department of Biology, 208 Mueller Laboratory, The Pennsylvania clusters (e.g., classes and below), they have also shown the State University, University Park, PA 16802-5301, USA; bCurrent susceptibility of eubacterial phylogeny to biases such as address: Center for Evolutionary Functional Genomics, The Biodesign horizontal gene transfer (HGT) (20, 21). Institute, Arizona State University, Tempe, AZ 85287-5301, USA In recent years, three major approaches have been used *To whom correspondence should be addressed (Fabia.Battistuzzi@ asu.edu) for studying prokaryote phylogeny with data from com- plete genomes: (i) combining gene sequences in a single analysis of multiple genes (e.g., 7, 9, 10), (ii) combining Abstract trees from individual gene analyses into a single “super- tree” (e.g., 22, 23), and (iii) using the presence or absence The ~9400 recognized species of prokaryotes in the of genes (“gene content”) as the raw data to investigate Superkingdom Eubacteria are placed in 25 phyla. Their relationships (e.g., 17, 18). While the results of these dif- relationships have been diffi cult to establish, although ferent approaches have not agreed on many details of some major groups are emerging from genome analyses. relationships, there have been some points of agreement, A molecular timetree, estimated here, indicates that most such as support for the monophyly of all major classes (85%) of the phyla and classes arose in the Archean Eon and some phyla (e.g., Proteobacteria and Firmicutes). (4000−2500 million years ago, Ma) whereas most (95%) of 7 ese A ndings, although criticized by some (e.g., 24, 25), the families arose in the Proterozoic Eon (2500−542 Ma). It suggest the presence of a detectable evolutionary sig- also points to an early origin of phototrophy (3400–3200 nal for prokaryotes when using carefully selected genes Ma) followed by colonization of land (3041–2755 Ma), origin (e.g., vertically inherited) and appropriate methodolo- of oxygenic photosynthesis (2920–2592 Ma) and of aerobic gies (e.g., genome-scale data sets). methanotrophy (2630–2371 Ma). 7 e Superkingdom Eubacteria (also called “Bacteria,” Fig. 1) is subdivided into 25 recognized phyla 1(), although other classiA cations have been proposed (2) and putative lineages await taxonomic assignment (e.g., 3, 4). In con- trast to most eukaryotic groups, eubacterial phylogeny has been di1 cult to resolve at the highest level (i.e., phyla and class relationships) despite the availability of many com- plete genome sequences. 7 e small subunit (SSU) ribo- somal RNA (rRNA) gene has been widely used to study prokaryote phylogeny and A rst revealed the distinction of eubacteria from archaebacteria (Archaea) (5, 6). However, because of its limited length and the large genetic dis- tances among prokaryote species, it is also subject to Fig. 1 Spirillum, a betaproteobacterium (upper left); Beggiatoa, biases such as long-branch attraction, base composition a gammaproteobacterium (upper right); an unidentifi ed diB erences, and a generally poor resolving power. 7 ese cyanobacterium (lower left); and an unidentifi ed spirochete (lower right). Credits: D. J. Patterson, L. Amaral-Zettler, and issues mostly have been addressed in more recent years V. Edgcomb (upper left and right); D. J. Patterson (lower left); by using genome-scale data sets (e.g., multiple genes, gene and L. Amaral-Zettler, L. Olendzenski, and D. J. Patterson (lower content, and insertion–deletion events) and increased right). Images provided by micro*scope (http://microscope.mbl. taxonomic sampling (7–19, 88). While these studies have edu) under creative commons license. F. U. Battistuzzi and S. B. Hedges. Eubacteria. Pp. 106–115 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, New York, 2009). HHedges.indbedges.indb 110606 11/28/2009/28/2009 11:25:27:25:27 PPMM Eubacteria 107 Staphylococcaceae 50 Bacillaceae 61 30 Listeriaceae Lactobacillaceae 54 21 Streptococcaceae Acholeplasmataceae 29 Mycoplasmataceae-1 46 Mycoplasmataceae-2 85 15 Entomoplasmataceae Firmicutes Symbiobacterium 24 Carboxydothermus 33 Peptococcaceae 44 8 20 Thermoanaerobacteriaceae-1 Clostridiaceae 36 Thermoanaerobacteriaceae-2 Dehalococcoides Terrabacteria 11 Gloeobacteraceae Chloroflexi 60 Synechococcaceae-1 66 Synechococcaceae-2 6 75 Synechococcaceae-3 76 Nostocaceae Cyanobacteria 80 Merismopediaceae Deinococcaceae Propionibacteriaceae Frankiaceae Deinococcus-Thermus 13 53 63 Corynebacteriaceae 82 Mycobacteriaceae 88 59 Nocardiaceae 43 Streptomycetaceae 69 Nocardiopsaceae Actinobacteria Bifidobacteriaceae 48 Cellulomonadaceae 71 Microbacteriaceae (continued on next page) Ea Pa Ma Na Pp Mp Np Pz HD ARCHEAN PROTEROZOIC PH 4000 3000 2000 1000 0 Million years ago Fig. 2 Continues HHedges.indbedges.indb 110707 11/28/2009/28/2009 11:25:29:25:29 PPMM 108 THE TIMETREE OF LIFE (continued from previous page) Francisellaceae Shewanellaceae 73 Vibrionaceae 77 42 Enterobacteriaceae 81 70 Pasteurellaceae Idiomarinaceae 74 Colwelliaceae 47 79 Pseudoalteromonadaceae 37 Moraxellaceae 57 Pseudomonadaceae 67 Hahellaceae 32 Gammaproteobacteria Coxiellaceae 51 Legionellaceae Chromatiaceae Hydrobacteria 38 4 Methylococcaceae 34 26 Piscirickettsiaceae 39 Xanthomonadaceae Neisseriaceae Rhodocyclaceae 55 68 Comamonadaceae 72 Burkholderiaceae 78 58 Alcaligenaceae Nitrosomonadaceae Betaproteobacteria 64 Hydrogenophilaceae (continued on next page) Ea Pa Ma Na Pp Mp Np Pz HD ARCHEAN PROTEROZOIC PH 4000 3000 2000 1000 0 Million years ago Fig. 2 Continues Phylogenetic analyses that have focused on subgroups ribosomal proteins, DNA-directed RNA polymerase of prokaryotes (e.g., classes) also have supported, con- subunits (30), genome trees (31), and gene content ana- sistently, particular groupings. For example, cyanobac- lysis (18). Other taxa, such as AquiA cae and 7 ermotogae, teria and low GC gram positives (Firmicutes) have been have been more di1 cult to place, appearing at the base united based on maximum likelihood (ML) mapping of of the tree in some analyses (4, 7, 9, 32) and in a higher, 21 orthologous genes (26); Fusobacteria is the most closely nested position in other analyses (10, 33, 34). related group to Firmicutes based on combined analyses Generally concordant relationships were found of SSU and large subunit (LSU) rRNA sequences and between past studies and a recent ML and Bayesian ana- ribosomal proteins (27); Bacteroidetes, Chlorobi, and lysis of multiple core gene sequences (88). In that study, Fibrobacteres form a group based on insertion–deletion a complete matrix of 25 vertically inherited orthologous analysis (28, 29); and Planctomycetacia, Chlamydiae, genes shared by 197 fully sequenced eubacteria and 21 and Spirochaetes form a group based on concatenated fully sequenced species of archaebacteria was built. HHedges.indbedges.indb 110808 11/28/2009/28/2009 11:25:29:25:29 PPMM Eubacteria 109 (continued from previous page) 17 Erythrobacteraceae 41 Rhodobacteraceae 45 Caulobacteraceae 56 Bradyrhizobiaceae Rhizobiaceae 65 86 35 Phyllobacteriaceae 84 Bartonellaceae 87 14 Brucellaceae 25 Rhodospirillaceae 49 Alphaproteobacteria Acetobacteraceae 3 SAR11 27 Anaplasmataceae 40 Rickettsiaceae 9 Solibacteraceae 16 Desulfovibrionaceae Acidobacteria Myxococcaceae 18 28 Hydrobacteria Bdellovibrionaceae 22 Pelobacteraceae 52 Geobacteraceae Deltaproteobacteria Deltaproteobacteria 5 Campylobacteraceae 62 2 Helicobacteraceae Chlamydiaceae 12 Chlorobiaceae Epsilonproteobacteria Chlamydiae Chlamydiae 23 Crenotrichaceae Chlorobi 31 Bacteroidaceae 7 83 Porphyromonadaceae 1 Bacteroidetes Planctomycetaceae 10 Spirochaetaceae 19 Leptospiraceae Planctomycetes Fusobacteriaceae Spirochaetes Aquificaceae Fusobacteria Thermotogaceae Aquificae Ea Pa Ma Na Pp Mp Np Pz Thermotogae HD ARCHEAN PROTEROZOIC PH 4000 3000 2000 1000 0 Million years ago Fig. 2 A timetree of eubacteria. Divergence times Thermoanaerobacteriaceae-1 (Moorella thermoacetica), are shown in Table 1. Codes for paraphyletic and/or Thermoanaerobacteriaceae-2 (Thermoanaerobacter polyphyletic groups are as follows: Mycoplasmataceae-1 tengcongensis). Abbreviations: Ea (Eoarchean), HD (Hadean), (Mycoplasma genitalium), Mycoplasmataceae-2 (Mycoplasma Ma (Mesoarchean), Mp (Mesoproterozoic), Na (Neoarchean), capricolum), Synechococcaceae-1 (Synechocococcus Np (Neoproterozoic), Pa (Paleoarchean), PH (Phanerozoic), Pp JA-2-3Ba), Synechococcaceae-2 (Thermosynechococcus (Paleoproterozoic), and Pz (Paleozoic). elongatus), Synechococcaceae-3 (Synechococcus elongatus), HHedges.indbedges.indb 110909 11/28/2009/28/2009 11:25:30:25:30 PPMM 110 THE TIMETREE OF LIFE Table 1. Divergence times (Ma) and their confi dence/credibility intervals (CI) among eubacteria. Timetree Estimates Timetree Estimates Node Time Ref. (7) This study Node Time Ref. (7) This study Time CI Time CI Time CI Time CI 1 4189 – – 4189 4200–4159 45 1498 – – 1498 1644–1351 2 4179 – – 4179 4197–4141 46 1482 – – 1482 1656–1313 3 3306 3186 3634–2801 3306 3447–3165 47 1481 1387 1763–1060 1481 1586–1372 4 3134 – – 3134 3265–2987 48 1436 – – 1436 1600–1270 5 2979 3096 3539–2723 2979 3116–2835 49 1432 – – 1432 1580–1283 6 2908 – – 2908 3041–2755 50 1429 1561 2012–1166 1429 1597–1269 7 2897 – – 2897 3040–2747 51 1420 – – 1420 1539–1297 8 2874 – – 2874 3012–2716 52 1413 – – 1413 1573–1257 9 2849 2800 3223–2452 2849 2983–2706 53 1402 – – 1402 1557–1241 10 2762 – – 2762 2926–2595 54 1392 – – 1392 1573–1223 11 2761 – – 2761
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