Molecular signatures for the Crenarchaeota and the Thaumarchaeota

Abstract

Crenarchaeotes found in mesophilic marine environments were recently placed into a new phylum of Archaea called the Thaumarchaeota. However, very few molecular characteristics of this new phylum are currently known which can be used to distinguish them from the Crenarchaeota. In addition, their relationships to deep-branching archaeal lineages are unclear. We report here detailed analyses of protein sequences from Crenarchaeota and Thaumarchaeota that have identified many conserved signature indels (CSIs) and signature proteins (SPs) (i.e., proteins for which all significant blast hits are from these groups) that are specific for these archaeal groups. Of the identified signatures 6 CSIs and 13 SPs are specific for the Crenarchaeota phylum; 6 CSIs and >250 SPs are uniquely found in various Thaumarchaeota (viz. Cenarchaeum symbiosum, Nitrosopumilus maritimus and a number of uncultured marine crenarchaeotes) and 3 CSIs and ~10 SPs are found in both Thaumarchaeota and Crenarchaeota species. Some of the molecular signatures are also present in Korarchaeum cryptofilum, which forms the independent phylum Korarchaeota. Although some of these molecular signatures suggest a distant shared ancestry between Thaumarchaeota and Crenarchaeota, our identification of large numbers of Thaumarchaeota-specific proteins and their deep branching between the Crenarchaeota and Euryarchaeota phyla in phylogenetic trees shows that they are distinct from both Crenarchaeota and Euryarchaeota in both genetic and phylogenetic terms. These observations support the placement of marine mesophilic archaea into the separate phylum Thaumarchaeota. Additionally, many CSIs and SPs have been found that are specific for different orders within Crenarchaeota (viz. Sulfolobales-3 CSIs and 169 SPs, Thermoproteales-5 CSIs and 25 SPs, Desulfurococcales-4 SPs, and Sulfolobales and Desulfurococcales-2 CSIs and 18 SPs). The signatures described here provide novel means for distinguishing the Crenarchaeota and the Thaumarchaeota and for the classification of related and novel species in different environments. Functional studies on these signature proteins could lead to discovery of novel biochemical properties that are unique to these groups of archaea.

Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea)

“…This observation is coincident with a hypothesis that marine autotrophic archaea are likely the representatives of an evolutionary lineage different from Crenarchaea (Brochier-Armanet et al, 2008;Gupta and Shami, 2010;Spang et al, 2010).…”

Phylogeny and molecular signatures for the phylum Thermotogae and its subgroups

“…Other species with indel b 0 d 1/100 0/100 0 d 0/100 1998, 2000; Griffiths and Gupta 2004;Singh and Gupta 2009;Gupta and Shami 2011). These results provide convincing evidence that the conserved CSIs in protein sequences, despite their locations in the surface loops, are highly reliable and stable genetic characteristics of different lineages and they are not commonly lost or acquired, as is erroneously assumed.…”

“…Thus, these exceptions could be caused by either LGTs or other non-specific causes such as incorrect information for the source species for some sequences. The species distribution profile of this CSI provides strong evidence that this indel is a highly reliable characteristic of the above noted phyla of Gram-negative bacteria and it occurred once in a common ancestor of them and since then it has not been lost from any species from these groups (Gupta 1998(Gupta , 2000Griffiths and Gupta 2004;Singh and Gupta 2009;Gupta and Shami 2011). At the same time, the absence of this CSI in all other bacterial phyla strongly indicates that the genetic change that gave rise to this CSI was a highly specific event and that similar changes, even though it involves a protein surface loop, do not occur randomly or frequently in different lineages.…”

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.…”