Phylogeny and molecular signatures for the phylum Thermotogae and its subgroups

Abstract

Thermotogae species are currently identified mainly on the basis of their unique toga and distinct branching in the rRNA and other phylogenetic trees. No biochemical or molecular markers are known that clearly distinguish the species from this phylum from all other bacteria. The taxonomic/evolutionary relationships within this phylum, which consists of a single family, are also unclear. We report detailed phylogenetic analyses on Thermotogae species based on concatenated sequences for many ribosomal as well as other conserved proteins that identify a number of distinct clades within this phylum. Additionally, comprehensive analyses of protein sequences from Thermotogae genomes have identified >60 Conserved Signature Indels (CSI) that are specific for the Thermotogae phylum or its different subgroups. Eighteen CSIs in important proteins such as PolI, RecA, TrpRS and ribosomal proteins L4, L7/L12, S8, S9, etc. are uniquely present in various Thermotogae species and provide molecular markers for the phylum. Many CSIs were specific for a number of Thermotogae subgroups. Twelve of these CSIs were specific for a clade consisting of various Thermotoga species except Tt. lettingae, which was separated from other Thermotoga species by a long branch in phylogenetic trees; Fourteen CSIs were specific for a clade consisting of the Fervidobacterium and Thermosipho genera and eight additional CSIs were specific for the genus Thermosipho. In addition, the existence of a clade consisting of the deep branching species Petrotoga mobilis, Kosmotoga olearia and Thermotogales bacterium mesG1 was supported by seven CSIs. The deep branching of this clade was also supported by a number of CSIs that were present in various Thermotogae species, but absent in this clade and all other bacteria. Most of these clades were strongly supported by phylogenetic analyses based on two datasets of protein sequences and they identify potential higher taxonomic grouping (viz. families) within this phylum. We also report 16 CSIs that are shared by either some or all Thermotogae species and some species from other taxa such as Archaea, Aquificae, Firmicutes, Proteobacteria, Deinococcus, Fusobacteria, Dictyoglomus, Chloroflexi and eukaryotes. The shared presence of some of these CSIs could be due to lateral gene transfers between these groups. However, no clear preference for any particular group was observed in this regard. The molecular probes based on different genes/proteins, which contain these Thermotogae-specific CSIs, provide novel and highly specific means for identification of both known as well as previously unknown Thermotogae species in different environments. Additionally, these CSIs also provide valuable tools for genetic and biochemical studies that could lead to discovery of novel properties that are unique to these bacteria.

Microbial systematics in the post-genomics era

“…Recent work from our lab has identified a large number of CSIs that are restricted to many higher taxonomic groups within the prokaryotes, such as: alpha-proteobacteria, gammaproteobacteria, epsilon-proteobacteria, Aquifiales, Chlamydia, Cyanobacteria, Deinococcus-Thermus, Bacteroidetes-Chlorobi, Actinobacteria, Thermotogae, Archaea, etc. (Gupta 2009;Gao et al 2009;Griffiths and Gupta 2004a, 2004bGriffiths et al 2005;Gupta 1998Gupta , 2004Gupta , 2010Gupta and Bhandari 2011;Gao and Gupta 2005;Gupta and Shami 2011;Naushad and Gupta 2011). These newly discovered CSIs provide useful markers for defining or circumscribing the above prokaryotic groups in clear molecular terms.…”

A call to arms for systematists: revitalising the purpose and practises underpinning the description of novel microbial taxa

“…The ability to analyse shared gene content at different taxonomic levels may also lead to a better ability to define taxa (based on consideration of the 'core genome' within the 'pan genome' (Mira et al 2010) such that we may eventually be able move to 'conceptual' prokaryotic taxon definitions based on genomic analysis. Recent studies of the core genome of representatives of the genus Streptococcus provide powerful illustrations of this approach (Lefébure and Stanhope 2007;Donati et al 2010), as does the use of molecular signatures (proteins and/or indels) to define higher taxa (Adék-ambi et al 2011;Gupta and Shami 2011;Gupta and Vaibhav 2011). However, the need for multiple genomes representing a taxon may limit the applicability of these analyses at the species level due to the accelerating trend for the description of single strain taxa (Felis and Dellaglio 2007).…”

Phylogeny and molecular signatures for the phylum Fusobacteria and its distinct subclades

“…37e40. The shared presence of CSIs in these unrelated groups could be caused by either lateral gene transfers or independent occurrence of similar genetic changes in these unrelated taxa [5,27,30,33]. However, as discussed in detail elsewhere these CSIs do not provide much useful information for understanding the evolutionary relationships within the phylum Fusobacteria and based upon them it is also not possible to deduce any specific relationship between Fusobacteria and any other bacterial phyla [33].…”