Molecular signatures for the class Coriobacteriia and its different clades; proposal for division of the class Coriobacteriia into the emended order Coriobacteriales, containing the emended family Coriobacteriaceae and Atopobiaceae fam. nov., and Eggerthellales ord. nov., containing the family Eggerthellaceae fam. nov.
The species of the class Coriobacteriia are currently distinguished from other bacteria primarily on the basis of their branching in the 16S rRNA gene trees. No reliable molecular marker is known that distinguishes the bacteria of this class from other organisms. We report here the results of detailed phylogenetic and comparative analyses on 22 sequenced genomes from members of the class Coriobacteriia. Detailed comparative analyses on protein sequences from these genomes, reported here, have identified 66 conserved signature inserts or deletions (i.e. indels) (CSIs) in widely distributed proteins that are specific for a number of different clades of the class Coriobacteriia at multiple phylogenetic levels, which are also supported by phylogenetic analyses. A set of 24 CSIs in different proteins are specific for all sequenced members of the class Coriobacteriia, providing novel molecular markers distinguishing and delimiting this class. One additional CSI is uniquely present in all members of the class Coriobacteriia and the phylum Actinobacteria supporting their placement within this bacterial phylum. A set of 16 CSIs in divergent proteins are uniquely found in the genomes of all species for which sequences are available from the glucose-fermenting genera Coriobacterium, Collinsella, Atopobium and Olsenella, but they are not present in any other bacteria. The species from these genera also form a strongly supported clade (Clade I) in the phylogenetic trees based upon concatenated protein sequences and the 16S rRNA. An additional 10 CSIs in different proteins are specifically present in all members of the asaccharolytic genera Eggerthella, Cryptobacterium, Slackia and Gordonibacter for which sequence data is available. A clade consisting of these genera (Clade II) is also supported by our phylogenetic analyses. Within Clade I, two smaller clades, one consisting of the genera Coriobacterium and Collinsella and the other containing the genera Atopobium and Olsenella, are independently supported by multiple CSIs (eight and seven respectively) and our phylogenetic analyses. Based upon the results of phylogenetic studies and the identified molecular markers, which clearly distinguish and demarcate the above indicated clades of the class Coriobacteriia at different phylogenetic depths, we propose division of the class Coriobacteriia into two orders (viz. Coriobacteriales and Eggerthellales ord. nov.) and three families (viz. Coriobacteriaceae, Atopobiaceae fam. nov. and Eggerthellaceae fam. nov.). Additionally, descriptions of the class Coriobacteriia, the order Coriobacteriales and the family Coriobacteriaceea are also emended.
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Funding
This study was supported by the:
Natural Science and Engineering Research Council of Canada
AndersonR. C.,
RasmussenM. A.,
JensenN. S.,
AllisonM. J.(2000).Denitrobacterium detoxificans gen. nov., sp. nov., a ruminal bacterium that respires on nitrocompounds. . Int J Syst Evol Microbiol50, 633–638. [View Article][PubMed]
CastresanaJ.(2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. . Mol Biol Evol17, 540–552. [View Article][PubMed]
CiccarelliF. D.,
DoerksT.,
von MeringC.,
CreeveyC. J.,
SnelB.,
BorkP.(2006). Toward automatic reconstruction of a highly resolved tree of life. . Science311, 1283–1287. [View Article][PubMed]
ClavelT.,
CharrierC.,
BrauneA.,
WenningM.,
BlautM.,
HallerD.(2009). Isolation of bacteria from the ileal mucosa of TNFdeltaARE mice and description of Enterorhabdus mucosicola gen. nov., sp. nov.. Int J Syst Evol Microbiol59, 1805–1812. [View Article][PubMed]
CollinsM. D.,
WallbanksS.(1992). Comparative sequence analyses of the 16S rRNA genes of Lactobacillus minutus, Lactobacillus rimae and Streptococcus parvulus: proposal for the creation of a new genus Atopobium
. . FEMS Microbiol Lett95, 235–240. [View Article][PubMed]
DewhirstF. E.,
PasterB. J.,
TzellasN.,
ColemanB.,
DownesJ.,
SprattD. A.,
WadeW. G.(2001). Characterization of novel human oral isolates and cloned 16S rDNA sequences that fall in the family Coriobacteriaceae: description of Olsenella gen. nov., reclassification of Lactobacillus uli as Olsenella uli comb. nov. and description of Olsenella profusa sp. nov.. Int J Syst Evol Microbiol51, 1797–1804. [View Article][PubMed]
EuzébyJ. P.(2012). List of bacterial names with standing in nomenclature: a folder available on the Internet. . [Last full update 8 June 2012]. www.bacterio.net.
GaoB.,
GuptaR. S.(2005). Conserved indels in protein sequences that are characteristic of the phylum Actinobacteria
. . Int J Syst Evol Microbiol55, 2401–2412. [View Article][PubMed]
GaoB.,
GuptaR. S.(2012b). Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria
. . Microbiol Mol Biol Rev76, 66–112. [View Article][PubMed]
GaoB.,
ParamanathanR.,
GuptaR. S.(2006). Signature proteins that are distinctive characteristics of Actinobacteria and their subgroups. . Antonie van Leeuwenhoek90, 69–91. [View Article][PubMed]
GuptaR. S.(1998). Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. . Microbiol Mol Biol Rev62, 1435–1491.[PubMed]
GuptaR. S.(2001). The branching order and phylogenetic placement of species from completed bacterial genomes, based on conserved indels found in various proteins. . Int Microbiol4, 187–202. [View Article][PubMed]
GuptaR. S.(2009). Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. . Int J Syst Evol Microbiol59, 2510–2526. [View Article][PubMed]
HaasF.,
KönigH.(1988).Coriobacterium glomerans gen. nov., sp. nov. from the intestinal tract of the red soldier bug. . Int J Syst Bacteriol38, 382–384. [View Article]
JonesD. T.,
TaylorW. R.,
ThorntonJ. M.(1992). The rapid generation of mutation data matrices from protein sequences. . Comput Appl Biosci8, 275–282.[PubMed]
KageyamaA.,
BennoY.(2000). Emendation of genus Collinsella and proposal of Collinsella stercoris sp. nov. and Collinsella intestinalis sp. nov.. Int J Syst Evol Microbiol50, 1767–1774.[PubMed][CrossRef]
KageyamaA.,
BennoY.,
NakaseT.(1999). Phylogenetic and phenotypic evidence for the transfer of Eubacterium aerofaciens to the genus Collinsella as Collinsella aerofaciens gen. nov., comb. nov.. Int J Syst Bacteriol49, 557–565. [View Article][PubMed]
KimuraM.(1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. . J Mol Evol16, 111–120. [View Article][PubMed]
KönigH.(2012). Class III. Coriobacteriia class. nov.. In Bergey's Manual of Systematic Bacteriology, pp. 1975–1976. Edited by
GoodfellowM.,
KämpferP.,
BusseH. J.,
TrujilloM. E.,
SuzukiK.,
LudwigW.,
WhitmanW. B.
. New York:: Springer;.
KumarS.,
NeiM.,
DudleyJ.,
TamuraK.(2008).mega: a biologist-centric software for evolutionary analysis of DNA and protein sequences. . Brief Bioinform9, 299–306. [View Article][PubMed]
LauS. K.,
WooP. C.,
WooG. K.,
FungA. M.,
WongM. K.,
ChanK. M.,
TamD. M.,
YuenK. Y.(2004).Eggerthella hongkongensis sp. nov. and Eggerthella sinensis sp. nov., two novel Eggerthella species, account for half of the cases of Eggerthella bacteremia. . Diagn Microbiol Infect Dis49, 255–263. [View Article][PubMed]
LudwigW.,
EuzébyJ.,
SchumannP.,
BusseH. J.,
TrujilloM. E.,
KämpferP.,
WhitmanW. B.(2012). Road map of the phylum Actinobacteria
. . In Bergey's Manual of Systematic Bacteriology, pp. 1–28. Edited by
GoodfellowM.,
KämpferP.,
BusseH. J.,
TrujilloM. E.,
SuzukiK.,
LudwigW.,
WhitmanW. B.
. New York:: Springer;. [View Article]
MaruoT.,
SakamotoM.,
ItoC.,
TodaT.,
BennoY.(2008).Adlercreutzia equolifaciens gen. nov., sp. nov., an equol-producing bacterium isolated from human faeces, and emended description of the genus Eggerthella
. . Int J Syst Evol Microbiol58, 1221–1227. [View Article][PubMed]
MolC. D.,
HarrisJ. M.,
McIntoshE. M.,
TainerJ. A.(1996). Human dUTP pyrophosphatase: uracil recognition by a β hairpin and active sites formed by three separate subunits. . Structure4, 1077–1092. [View Article][PubMed]
NagaiF.,
WatanabeY.,
MorotomiM.(2010).Slackia piriformis sp. nov. and Collinsella tanakaei sp. nov., new members of the family Coriobacteriaceae, isolated from human faeces. . Int J Syst Evol Microbiol60, 2639–2646. [View Article][PubMed]
NakazawaF.,
PocoS. E.,
IkedaT.,
SatoM.,
KalfasS.,
SundqvistG.,
HoshinoE.(1999).Cryptobacterium curtum gen. nov., sp. nov., a new genus of Gram-positive anaerobic rod isolated from human oral cavities. . Int J Syst Bacteriol49, 1193–1200. [View Article][PubMed]
Rodriguez JovitaM.,
CollinsM. D.,
SjödénB.,
FalsenE.(1999). Characterization of a novel Atopobium isolate from the human vagina: description of Atopobium vaginae sp. nov.. Int J Syst Bacteriol49, 1573–1576. [View Article][PubMed]
StackebrandtE.,
SchumannP.
( 2006;). Introduction to the taxonomy of Actinobacteria
. . In The Prokaryotes, , 3rd edn., vol. 3, pp. 297–321. Edited by
DworkinM.,
FalkowS.,
RosenbergE.,
SchleiferK. H.,
StackebrandtE.
. New York:: Springer;. [View Article]
StackebrandtE.,
RaineyF. A.,
Ward-RaineyN. L.(1997). Proposal for a new hierarchic classification system, Actinobacteria classis nov.. Int J Syst Bacteriol47, 479–491. [View Article]
WadeW. G.,
DownesJ.,
DymockD.,
HiomS. J.,
WeightmanA. J.,
DewhirstF. E.,
PasterB. J.,
TzellasN.,
ColemanB.(1999). The family Coriobacteriaceae: reclassification of Eubacterium exiguum (Poco et al. 1996) and Peptostreptococcus heliotrinreducens (Lanigan 1976) as Slackia exigua gen. nov., comb. nov. and Slackia heliotrinireducens gen. nov., comb. nov., and Eubacterium lentum (Prevot 1938) as Eggerthella lenta gen. nov., comb. nov.. Int J Syst Bacteriol49, 595–600. [View Article][PubMed]
WhelanS.,
GoldmanN.(2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. . Mol Biol Evol18, 691–699. [View Article][PubMed]
WürdemannD.,
TindallB. J.,
PukallR.,
LünsdorfH.,
StrömplC.,
NamuthT.,
NahrstedtH.,
Wos-OxleyM.,
OttS.& other authors (2009).Gordonibacter pamelaeae gen. nov., sp. nov., a new member of the Coriobacteriaceae isolated from a patient with Crohn’s disease, and reclassification of Eggerthella hongkongensis Lau et al. 2006 as Paraeggerthella hongkongensis gen. nov., comb. nov.. Int J Syst Evol Microbiol59, 1405–1415. [View Article][PubMed]
YarzaP.,
RichterM.,
PepliesJ.,
EuzebyJ.,
AmannR.,
SchleiferK. H.,
LudwigW.,
GlöcknerF. O.,
Rosselló-MóraR.(2008). The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. . Syst Appl Microbiol31, 241–250. [View Article][PubMed]
ZhiX. Y.,
LiW. J.,
StackebrandtE.(2009). An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. . Int J Syst Evol Microbiol59, 589–608. [View Article][PubMed]
Molecular signatures for the class Coriobacteriia and its different clades; proposal for division of the class Coriobacteriia into the emended order Coriobacteriales, containing the emended family Coriobacteriaceae and Atopobiaceae fam. nov., and Eggerthellales ord. nov., containing the family Eggerthellaceae fam. nov.