Phylogenomic analysis of proteins that are distinctive of Archaea and its main subgroups and the origin of methanogenesis
© Gao and Gupta; licensee BioMed Central Ltd. 2007
Received: 26 July 2006
Accepted: 29 March 2007
Published: 29 March 2007
The Archaea are highly diverse in terms of their physiology, metabolism and ecology. Presently, very few molecular characteristics are known that are uniquely shared by either all archaea or the different main groups within archaea. The evolutionary relationships among different groups within the Euryarchaeota branch are also not clearly understood.
We have carried out comprehensive analyses on each open reading frame (ORFs) in the genomes of 11 archaea (3 Crenarchaeota – Aeropyrum pernix, Pyrobaculum aerophilum and Sulfolobus acidocaldarius; 8 Euryarchaeota – Pyrococcus abyssi, Methanococcus maripaludis, Methanopyrus kandleri, Methanococcoides burtonii, Halobacterium sp. NCR-1, Haloquadratum walsbyi, Thermoplasma acidophilum and Picrophilus torridus) to search for proteins that are unique to either all Archaea or for its main subgroups. These studies have identified 1448 proteins or ORFs that are distinctive characteristics of Archaea and its various subgroups and whose homologues are not found in other organisms. Six of these proteins are unique to all Archaea, 10 others are only missing in Nanoarchaeum equitans and a large number of other proteins are specific for various main groups within the Archaea (e.g. Crenarchaeota, Euryarchaeota, Sulfolobales and Desulfurococcales, Halobacteriales, Thermococci, Thermoplasmata, all methanogenic archaea or particular groups of methanogens). Of particular importance is the observation that 31 proteins are uniquely present in virtually all methanogens (including M. kandleri) and 10 additional proteins are only found in different methanogens as well as A. fulgidus. In contrast, no protein was exclusively shared by various methanogen and any of the Halobacteriales or Thermoplasmatales. These results strongly indicate that all methanogenic archaea form a monophyletic group exclusive of other archaea and that this lineage likely evolved from Archaeoglobus. In addition, 15 proteins that are uniquely shared by M. kandleri and Methanobacteriales suggest a close evolutionary relationship between them. In contrast to the phylogenomics studies, a monophyletic grouping of archaea is not supported by phylogenetic analyses based on protein sequences.
The identified archaea-specific proteins provide novel molecular markers or signature proteins that are distinctive characteristics of Archaea and all of its major subgroups. The species distributions of these proteins provide novel insights into the evolutionary relationships among different groups within Archaea, particularly regarding the origin of methanogenesis. Most of these proteins are of unknown function and further studies should lead to discovery of novel biochemical and physiological characteristics that are unique to either all archaea or its different subgroups.
Archaea are widely regarded as one of the three main domains of life [1–7], although their origin is a subject of debate [8–14]. Archaeal species were earlier believed to inhabit only extreme environments such as extremely hot, or hot and acidic, extremely saline, or very acidic or alkaline conditions [15–19]. However, recent studies provide evidence that they are widespread in different environments [3, 20]. The archaea also include methanogens, which grow under strictly anaerobic and often thermophilic conditions, and are the only organisms that derive all of their metabolic energy by reduction of CO2 by hydrogen to produce methane [21, 22]. The archaeal species branch distinctly from all other organisms in phylogenetic trees based on 16S rRNA and many other gene/protein sequences [2, 7, 23–25]. In addition, many morphological or physiological characteristics such as the presence of branched-chain ether-linked lipids in their cell membrane, lack of peptidoglycan in their cell wall, characteristic subunit pattern of RNA polymerase, presence of modified bases in tRNA, presence of a unique form of DNA polymerase, have been previously indicated as defining characteristics of archaea [1, 15]. However, as noted by Walsh and Doolittle , many of these features are either not shared by all archaea or they are also present in various eukaryotes or some thermophilic bacteria, indicating that they do not constitute distinctive characteristics of all Archaea.
Genome sizes, protein numbers and GC content of sequenced archaeal strains.
Genome Size (Mb)
GC content (%)
Pyrobaculum aerophilum str. IM2
Aeropyrum pernix K1
Sulfolobus acidocaldarius DSM 639
Sulfolobus solfataricus P2
Sulfolobus tokodaii str. 7
Thermococcus kodakarensis KOD1
Pyrococcus abyssi GE5
Pyrococcus horikoshii OT3
Pyrococcus furiosus DSM 3638
Methanopyrus kandleri AV19
Methanosphaera stadtmanae DSM 3091
Methanococcus maripaludis S2
Methanocaldococcus jannaschii DSM 2661
Methanospirillum hungatei JF-1
Methanosaeta thermophila PT
Methanococcoides burtonii DSM 6242
Methanosarcina acetivorans C2A
Methanosarcina mazei Go1
Methanosarcina barkeri str. fusaro
Archaeoglobus fulgidus DSM 4304
Halobacterium sp. NRC-1
Haloarcula marismortui ATCC 43049
Haloquadratum walsbyi DSM 16790
Natronomonas pharaonis DSM 2160
Picrophilus torridus DSM 9790
Thermoplasma acidophilum DSM 1728
Thermoplasma volcanium GSS1
Nanoarchaeum equitans Kin4-M
Whole proteins that are uniquely present in particular groups or subgroups of organisms but not found anywhere else provide valuable molecular markers for taxonomic, phylogenetic and biochemical studies. These proteins, which we refer to as signature proteins in our work, and others have called them as ORFans or conserved hypothetical proteins, are present at different phylogenetic depths, such as genus, family, order or even phylum [35, 36, 38–42]. In our recent work, a large number of such proteins that are distinctive characteristics of several groups within bacteria (viz. α-proteobacteria, ε-proteobacteria, Chlamydia and Actinobacteria), and also their subgroups, were identified [39–43]. These proteins provide not only valuable molecular markers for identifying and circumscribing species belonging to these major groups (and their subgroups) in molecular terms, but their species distribution pattern also provides useful information about the branching order within these groups. As archaea constitute a very diverse group, identification of sets of proteins that are specific for its main groups and subgroups should prove useful in terms of identifying molecular characteristics that are unique to them. Additionally, this information should also be helpful in understanding the evolutionary relationships among different groups.
Comparative studies on limited numbers of archaeal genomes have been carried out by a number of investigators using different criteria. Graham et al.  analyzed 9 archaeal genomes to identify signature proteins that function uniquely within the Archaea. Their definition of an archaeal signature protein required it to be present in only two different euryarchaeal species and they identified 353 archaeal signature proteins. Makarova and Koonin [27, 35] have analyzed archaeal genomes to identify core sets of genes, which are present in all archaeal species, but which are not restricted to the archaeal species. Recently, Walsh and Doolittle have analyzed prokaryotic genomes to measure dissimilarity between Archaea and Bacteria . Although it was reported that 28% of the proteins from archaeal genomes are restricted to the Archaea, specific proteins that were present in different groups of archaea were not identified. Other comparative studies using different criteria have been conducted on smaller groups within archaea such as Pyrococcus, Sulfolobus and thermoacidophilic organisms (to be discussed later). However, thus far no comprehensive phylogenomics study on different archaeal genomes has been carried out using the same standard criteria to identify proteins or ORFs that are shared by all archaea or its different major lineages. In this study we have carried out comparative analyses of archaeal genomes using uniform criteria to identify proteins that are uniquely present in archaeal species at different phylogenetic depths (genus or higher) representing all major groups within the Archaea.
Results and discussion
A. Phylogenetic analyses of archaeal species
Prior to undertaking comparative studies on archaeal genomes, phylogenetic analysis of sequenced archaeal species was carried out so that the results of phylogenomics analyses could be compared with those obtained by traditional phylogenetic approaches. Phylogenetic trees for the archaeal species based on 16S rRNA as well as concatenated sequences of translation and transcription-related proteins have been published by other investigators [7, 28, 32, 44]. In the present work, we have constructed phylogenetic trees for 29 archaeal species (see Table 1) using a set of 31 universally distributed proteins that are involved in a broad range of functions . The sequence of Haloquadratum walsbyi DSM 16790, which became available afterward, was not included in these studies. Phylogenetic trees based on a concatenated sequence alignment of these proteins were constructed using the neighbour-joining (NJ), maximum-likelihood (ML) and maximum-parsimony (MP) methods.
B. Phylogenomic analyses of archaeal genomes
To search for proteins (or ORFs), which are uniquely present in either all Archaea or various subgroups of them, blast searches were performed on each open reading frame (ORF) from a total of 11 archaeal genomes (see Table 1; shaded species in Fig. 1). These genomes included 3 Crenarchaeota (viz. Aeropyrum pernix, Pyrobaculum aerophilum and Sulfolobus acidocaldarius) [49–51] and 8 divergent Euryarchaeota species covering all main functional and phylogenetic groups (see Table 1 and Fig. 1). The Euryarchaeota genomes analyzed included: Pyrococcus abyssi from extremely thermophilic sulfur metabolizing archaea , Methanococcus maripaludis  from Methanococcales, Halobacterium sp. NRC-1 and H. walsbyi from extreme halophiles , Thermoplasma acidophilum and Picrophilus torridus belonging to the cell wall-less archaea [19, 55], Methanococcoides burtonii from Methanosarcinales and Methanopyrus kandleri from the Methanopyrales order . The chosen genomes should provide information regarding all archaeal proteins that are shared at a taxonomic level higher than a genus. The analysis of the remainder of the genomes, which was expected to provide information regarding proteins that are only unique to a given species, was not carried out.
Proteins that are specific for all Archaea
(a) Proteins specific to all Archaea
(b) Archaea-specific proteins with gene loss in few species
Proteins that are specific for Crenarchaeota
(a) Proteins specific to Crenarchaeota
(b) Proteins specific to Aeropyrum and Sulfolobus
(c) Proteins specific to Aeropyrum and Pyrobaculum
(d) Proteins specific to Sulfolobus and Pyrobaculum
Proteins that are specific for Euryarchaeota
(a) Proteins specific to almost all Euryarchaeota
Pol II COG1933
(b) Proteins specific to Euryarchaeota except Thermoplasmata
Proteins that are specific for methanogens (Methanoarchaeota)
(a) Proteins specific to Methanoarchaeota
(b) Proteins specific to all methanogen and A. fulgidus
(c) Proteins specific to some methanogen and A. fulgidus
Proteins that are specific to certain subgroups of methanogens
(a) Proteins specific to Methanococcales, Methanobacteriales, Methanopyrales and Methanomicrobiales
(b) Proteins specific to Methanococcales, Methanobacteriales and Methanopyrales
(c) Proteins specific to Methanobacteriales and Methanopyrales
[NP_614882] = MK0927
[NP_614565] = MK0502
(d) Proteins specific to Methanosarcinales
(e) Proteins only found in Methanococcales and Methanobacteriales
(f) Proteins only found in Methanococcales and Methanopyrales
(g) Proteins only found in Methanosarcinales and Methanomicrobiales
Proteins restricted to several archaeal lineages
(a) Proteins only found in Thermococci, Archaeoglobus and methanogens
(b) Proteins unique to Thermococci + Archaeoglobus
(c) Proteins mainly shared by Halobacteria and some methanogens
(d) Proteins mainly shared by Thermoplasmata and Sulfolobus
(a) Proteins that are specific for all Archaea
Of the proteins that are uniquely present in all archaea, PAB0063 corresponds to tRNA nucleotidyltransferase (CCA-adding enzyme), which builds and repairs the 3' end of tRNA . Functionally similar enzymes are also present in bacteria and eukaryotes (assigned as Class II), but their sequences share very little homology with the archaeal CCA-adding enzyme (Class I), which explains why no homologs were detected in any bacteria or eukaryotes in blast searches. The main mechanistic difference between class I and class II enzymes is that the tRNA substrate is required to fully define the nucleotide binding site in class I enzyme, whereas class II has a preformed nucleotide binding site that recognizes CTP and ATP in the absence of tRNA . Another protein PAB0316 is assigned as archaeal type DNA primase, which also has its synonymous counterparts in bacterial and eukaryotic species, but shows very little homology to them [61, 62]. In the same way, protein PAB1633 is annotated as a PilT family ATPase, which showed very little similarity to bacterial ATPases involved in type IV pili biogenesis . Further studies of this protein could provide insights into novel aspects of the archaeal flagellar system. A number of other proteins viz. PAB1716, PAB0018a, PAB0075, PAB0475 and PAB2104, have also been assigned putative functions based on sequence analysis, but their exact roles in archaeal cells remains to be determined. Interestingly, for protein PAB0075, two gene copies with acceptable E-values are also present in the genomes of Dehalococcoides ethenogenes 195, Dehalococcoides sp. CBDB1 and Dehalococcoides sp. BAV1, which belong to Chloroflexi . Because no homologue of PAB0075 is present in other bacteria, it is likely that this protein was transferred from archaea to the common ancestor of Dehalococcoides followed by a gene duplication event.
Table 2(b) lists 20 additional proteins, which are specific to archaea but missing in a small number of species. Because these proteins are present in most Euryarchaeota as well as Crenarchaeota species, but not detected in Bacteria or Eukaryotes except one LGT case (PAB2342, see note in Table 2), we consider them also to be distinctive characteristics of most Archaea. Of these proteins, 11 proteins (viz. PAB0654, PAB0950, PAB1135, PAB1906, PAB7388, PAB0547, PAB0552, PAB0623, PAB1272, PAB1429 and PAB1721) are mainly missing in the 4 Thermoplasmata species. Thermoplasmata are thermoacidophilic archaea which lack cell envelope [19, 55, 63](see Table 1). Some studies have suggested that high temperature and very low intracellular pH exert selective pressure favouring smaller genomes . Thus, it is possible that genes for these proteins were selectively lost in the Thermoplasmata lineage. Most of these proteins are of unknown function. However, 8 of them have been assigned putative functions with the title of "archaeal type"'. For example, PAB0301 is archaeal sugar kinase, PAB0950 is archaeal transcription factor E α-subunit, PAB1387 is archaeal flagella accessory protein, PAB7094 is archaeal chromatin protein, and PAB0552 is archaeal type Holliday junction resolvase. These proteins do not show detectable sequence similarity to their counterparts in Bacteria or Eukaryotes, and some studies indicate that they also differ in terms of their structure, function or interaction with other cell components [64, 65].
(b) Proteins that are specific for Crenarchaeota
As mentioned in the introduction, the Archaea are divided into 2 main groups, Crenarchaeota and Euryarchaeota, based on 16S rRNA trees as well many other gene trees and characteristics. The Crenarchaeota are also indicated to differ from Euryarchaeota in terms of their ribosome structure [30, 31]. In comparison to Euryarchaeota, which contain physiologically and metabolically diverse groups of organisms, the Crenarchaeota were thought to be a pure collection of extreme thermophiles and most members metabolize sulfur. However, recent studies indicate that Crenarchaeota are much more diverse in their physiology and ecology than was previously believed [28, 66]. Many species living in the cold ocean also belong to this group based on their branching pattern in 16S rRNA trees, although most of them have not been cultivated . Currently, this phylum is comprised of one single class Thermoprotei containing three orders: Thermoproteales, Desulfurococcales and Sulfolobales. Fortunately, every order has a completely sequenced representative (see Table 1)[50, 51, 68, 69], which provide a platform to explore the characteristics that are unique to crenarchaeal species. Comparative genomic surveys have revealed some molecular features that are shared by crenarchaea but not euryarchaea, such as the lack of histones, absence of the FtsZ-MinCDE system and distinctive rRNA operon organization . Lake et al. have also identified distinctive differences in ribosome structure and an insert in elongation factor EF-G and EF-Tu, which can be used to distinguish Crenarchaeota from Euryarchaeota [6, 30, 70]. However, these features are not unique characteristics of the Crenarchaeota.
Blast searches on each ORF from the genomes of A. pernix and S. acidocaldarius DSM 639 [49, 50] have identified 11 proteins which are shared by all five crenarchaeal species, but whose homologs are not found in other archaea, or any bacteria or eukaryotes with only 3 exceptions (see Table 3(a)). The genes for these proteins likely evolved in a common ancestor of the Crenarchaeota and they provide potential molecular markers for species from this phylum. Additionally, 22 proteins that are listed in Table 3(b) are only found in A. pernix and three Sulfolobus genomes. These proteins suggest that Aeropyrum and Sulfolobus may have shared a common ancestor exclusive of Pyrobaculum. However, we have also come across 9 proteins that are shared by Aeropyrum and Pyrobaculum (Table 3(c)) and 14 proteins that are exclusively present in the 3 Sulfolobus species and Pyrobaculum (see Table 3(d)). Hence, based upon the species distributions of these proteins, the relationships among the Aeropyrum, Sulfolobales and Pyrobaculum are not entirely clear (Fig. 2a). In phylogenetic trees Thermoproteales (i.e. Pyrobaculum) branches consistently earlier than Desulfurococcales (i.e. Aeropyrum) and Sulfolobales (Fig. 1) [32, 44]. This observation in conjunction with the fact that Aeropyrum and Sulfolobus share larger numbers of proteins in common with each other suggests that these two groups likely shared a common ancestor exclusive of Pyrobaculum (Fig. 2b). The proteins that are only found in Aeropyrum and Pyrobaculum, or in Sulfolobus and Pyrobaculum, most likely evolved in a common ancestor of the crenarchaea, but were subsequently lost in either the Sulfolobales or A. pernix lineages.
In addition to these proteins that are uniquely present in either all sequenced Crenarchaeota genomes or different groups of Crenarchaeota species, these analyses have also identified 264 proteins that are unique for the Sulfolobales species (see Additional file 1). Of these, 184 proteins are present in all 3 sequenced Sulfolobus genomes, whereas the remaining 80 are present in at least two of the three Sulfolobus genomes. In this work, since blast analyses were not carried out on all three Sulfolobus genomes, it is likely that the numbers of genes or proteins that are uniquely shared by only two Sulfolobus genomes is much higher than indicated here. Chen et al.  have previously analyzed the genome of S. acidocaldarius DSM 639 and indicated the presence of 107 genes that were specific for Crenarchaeota and 866 genes that were specific to Sulfolobus genus. However, in the present work, relatively few genes that are uniquely shared by various Crenarchaeota species were identified. This difference could be due to more stringent criteria that we have employed for identification of proteins that are specific to different groups. The genome of Thermofilum pendens Hrk 5, which belongs to Thermoproteales, has also been partially sequenced and information for large numbers of genes/proteins from this species is available in the NCBI database. By carrying out blast searches on each ORF from P. aerophilum genome , we have identified 42 proteins that are only found in the above 2 Thermoproteales species (see Additional file 2). The numbers of proteins shared by these two species will likely increase once complete genome of T. pendens becomes available. Many of these proteins are expected to provide markers for the Thermoproteales order.
(c) Proteins that are specific for Euryarchaeota
The Euryarchaeota, which comprise a majority of the cultured and sequenced archaea, is a morphologically, metabolically and physiologically diverse collection of species as evidenced by the presence in this group of various methanogens, extreme halophiles, cell wall-less archaea and sulfate reducing microbes [2, 13]. No unique biochemical or molecular characteristic that is commonly shared by all of the different lineages is known. The present study has identified 20 proteins that are only found in Euryarchaeota species with 3 exceptions (see Table 4). In this Table, the first 7 proteins (Table 4(a)) are present in most euryarchaeota species. Of these proteins, PAB0082 and PAB2404 were found in all sequenced euryarchaeota species. PAB2404 was also present in N. equitans, supporting its placement within the Euryarchaeota [35, 46]. The protein PAB0082 is annotated as archaeosine tRNA-ribosyltransferase (ArcTGT), which catalyzes the exchange of guanine with a free 7-cyano-7-deazaguanine (preQ0) base, as the first step in the biosynthesis of an archaea-specific modified base, archaeosine (7-formamidino-7-deazaguanosine) . It should be mentioned that there is another protein PAB0740 in the same genome, which is also annotated and experimentally confirmed as ArcTGT . The latter belongs to a family of proteins that are highly conserved in all archaea species (including Crenarchaeota) and some bacteria. It seems that PAB0082 might be involved in RNA modification since it possesses a PUA domain (named after pseudouridine synthase and archaeosine transglycosylase), but its function is likely different from PAB0740. The protein PAB2404, which is annotated as DNA polymerase II large subunit, is highly conserved within Euryarchaeota, but is not found anywhere else except in Nanoarchaeum. This enzyme is the major DNA replicase in Euryarchaeota and also a distinctive molecular marker for this group [73, 74]. The genes for the above proteins likely evolved in a common ancestor of Euryarchaeota (Fig. 2) and they provide molecular markers for this diverse group of organisms.
Another 13 proteins listed in Table 4(b) are found in almost all euryarchaeota, but they are missing in Thermoplasmata. Their distribution suggests that either Thermoplasmata is a deep branching lineage within Euryarchaeota or that the genes for these proteins have been selectively lost from Thermoplasmata . Of these proteins, PAB0188 is also present in N. equitans supporting its placement with Euryarchaeota. Five other proteins from the first two columns in Table 4 (viz. MMP0243, Ta0062, VNG1263c, MMP1287, and VNG2408c) are also not found in the 4 Thermococci species. These results can again be explained by either selective loss of these genes from these particular groups or deeper branching of these lineages within the Euryarchaeota species. On the basis of proteins listed in Table 4, although one can infer that Thermoplasmata and Thermococci are deeper branching lineages within Euryarchaeota in comparison to methanogens, their relative branching order cannot be resolved.
(d) Proteins that are specific for different main groups within Euryarchaeota
Proteins specific for methanogenic archaea and their various subgroups
Currently, the methanogens form the largest group within the Euryarchaeota. They are distinguished from all other prokaryotes by their ability to obtain all or most of their energy via the reduction of CO2 to methane or by the process of methanogenesis. In the Bergey's manual , the methanogenes are divided into 5 distinct orders (viz. Methanobacteriales, Methanococcales, Methanomicrobiales, Methanosarcinales and Methanopyrales). Some studies have suggested that these organisms possess a set of unique enzymes which are responsible for methanogenesis, such as coenzyme M, Factor 420 and methanopterin . However, no systematic study has been carried out thus far to identify proteins that are uniquely present in different methanogens. Our blast searches of proteins from different methanogens have led to identification of 31 proteins, which are uniquely found in various methanogenic archaea. Twenty of these 31 proteins are present in all sequenced methanogens, while 11 proteins are missing only in M. stadtmanae, which is a human intestinal inhabitant (see notes in Table 5). This archaeon generate methane by reduction of methanol with H2 and lacks many proteins present in the genomes of other methanogens [77, 78]. Thus, it is highly likely that the 11 proteins missing in M. stadtmanae were selectively lost from this species. Therefore, it is very likely that the genes for these 31 proteins that are commonly shared by virtually all methanogens (Table 5(a)) evolved in a common ancestor of all methanogens.
Among the genes that are uniquely shared by various methanogenic archaea (or these archaea plus A. fulgidus), two large gene clusters responsible for methanogenesis are found. The proteins MMP1346, MMP1560–MMP1564 and MMP1566–MMP1567 (Table 5) are parts of an eight-component complex, coenzyme M methyltransferase (Mtr), which catalyzes an energy-conserving, sodium-ion-translocating step in methanogenesis from H2 and CO2 . M. maripaludis contains all of the known Mtr subunits, but the gene coding for MtrF is fused into the N-terminal region of MtrA . All other methanogenic archaeal genomes contain complete set of mtr genes. It is of interest to note that for the protein MMP1567 (MtrH), homologues with low E-values are also found in two Desulfitobacterium hafniense strains as well as in three Rhizobiales species (Aminobacter lissarensis, Methylobacterium chloromethanicum, and Hyphomicrobium chloromethanicum; α-proteobacteria) (see note in Table 5). These three rhizobiae species can use methyl halides as a sole source of carbon and energy, and all of them possess a set of cmu genes which are essential for methyl chloride degradation . In particular, the CmuB protein which is homologous to MMP1567 transfers a methyl group to methylcobalamin:H4 folate (H4F), which is analogous to the reverse of the reaction catalyzed by MtrH in archaea . In view of the sequence and functional similarity between MtrH and CmuB proteins, it is likely that the mtrH gene was laterally transferred from a methanogenic archaeon to the common ancestor of the above three rhizobiae species to serve the new functional role. The function of the laterally transferred mtrH related gene in D. hafniense is not known at present.
The proteins MMP1555–MMP1559 in Table 5 form another gene cluster, encoding the subunits of Methyl-coenzyme M reductase (MCR). This complex catalyzes the final reaction of the energy conserving pathway in which methylcoenzyme M and coenzyme B are converted to methane and the heterodisulfide CoM-S-S-CoB [87, 88]. Except for these proteins, the other proteins listed in Table 5 are of putative or unknown functions. It is likely that these proteins are involved in some aspects of methanogenesis or other unknown pathways unique to methanogenic archaea. These proteins provide molecular markers for methanogens, which can be used for identification of new archaeal species capable of methane production.
The blast searches of the M. maripaludis  and M. kandleri  genomes have identified 10 proteins that are uniquely shared by all of the following species belonging to the orders Methanobacteriales (M. thermoautotrophicus), Methanococcales (M. jannaschii, M. maripaludis) and Methanopyrales (M. kandleri) (Table 6(b)). Of these, only 2 proteins are present in M. stadtmanae, which is also a Methanobacteriales that has lost most of its genes due to its adaptation to the human intestine . The genes for these 10 proteins likely evolved in a common ancestor of the above groups of methanogens (Fig. 3), which corresponds to the cluster of methanogenic archaea referred to as "Class I methanogens" . Interestingly, these studies have also identified 10 proteins that are uniquely shared by these methanogenic orders and M. hungatei (see Table 6(a)), which branches distantly in phylogenetic trees . The unique presence of these proteins in these methanogens suggests that species from these groups shared a common ancestor exclusive of other methanogenic archaea (Fig. 3).
Fifteen additional proteins discovered in this work (Table 6(c)) are uniquely present in M. kandleri and various Methanobacteriales indicating that these two groups are more closely related to each other than the Methanococcales (Fig. 3). We have also come across 7 proteins that are uniquely shared by Methanococcales and Methanobacteriales (Table 6(d)), and 4 proteins that are only present in Methanococcales and Methanopyrales (Table 6(e)). The most likely explanation to account for the species distributions of these latter proteins is that their genes also originated in a common ancestor of the above three groups of methanogens, but were selectively lost in either the Methanobacteriales or Methanopyrales lineages. These analyses have also identified 14 additional proteins that are uniquely present in all 5 Methanosarcinales species (Table 6(f)), as well as 7 proteins that are only found in various Methanosarcinales and M. hungatei (Table 6(g)). Lastly, these studies have also identified 55 proteins that are uniquely present in M. maripaludis and M. jannaschii (Methanococcales, see Additional file 3(a)) and 68 proteins that are only present in M. burtonii and 3 Methanosarcina species, all belonging to the Methanosarcinaceae family (see Additional file 3(b)) (Fig. 3) indicating that they are likely distinctive characteristics of species from these groups.
Of the proteins that are uniquely found in Methanococcales, Methanobacteriales, Methanopyrales and Methanomicrobiales, 12 proteins viz. MMP1448–MMP1454, MMP1456, MMP1458–MMP1460 and MMP1467 are from a big gene cluster eha, which encodes the multisubunit membrane-bound [Ni-Fe] hydrogenase . Two of these proteins, MMP1456 and MMP1458, are only found in Methanococcales (Table 6(e)). The whole eha operon is composed of 20 ORFs in the genome of M. thermoautotrophicus and of these only these 12 proteins are restricted to these methanogens while the other subunits have counterparts in bacteria. The precise roles of these 12 proteins, which are predicted to be integral membrane proteins in the hydrogenase complex, have not been determined . Among the other proteins that are specific for these groups of methanogens, MMP0127 and MMP1716 are Hmd homologs, which catalyze the reversible dehydrogenation of N5, N10-methylenetetrahydromethanopterin . In the proteins that are specific for the Methanococcales (see Additional file 3(a)), one large gene cluster (MMP0233–MMP0240) is found, but no information is available concerning its possible function. Except for these proteins, all other proteins that are specific for these methanogenic archaea are of unknown or putative function.
Proteins that are specific for Thermococci
Thermococci are obligately thermophilic, strictly anaerobic cocci, which are able to convert elemental sulfur to hydrogen sulfide. Thus, they are so called "extremely thermophilic sulfur metabolizer", which comprise one of the main functional groups within Euryarchaeota. According to the Bergey's Manual , the class Thermococci contains only one family, Thermococcaceae, consisting of 2 genera: Thermococcus and Pyrococcus. Currently, 4 species from this family have been completely sequenced (Pyrococcus abyssi, P. horikoshii, P. furiosus and Thermococcus kodakarensis; see Table 1) [52, 91–93]. The blast searches on each protein from P. abyssi have identified 141 proteins that are shared by all 4 of these species (see Additional file 4(a)). All of these proteins show high degree of conservation within Thermococci and they do not have homologs in any other prokaryotes or eukaryotes except one possible LGT event (PAB1493, see note in Additional file 4). The genes for these proteins have likely evolved in a common ancestor of the Thermococci (Fig. 3). Of these proteins, PAB1510 is annotated as TBP-interacting protein (TIP), which forms complex with TBP (TATA-binding protein) to regulate transcription . It is known that the archaeal transcription machinery is strikingly similar to that in eukaryotes , but no TBP-binding component was found in archaeal species until the discovery of the TIP in T. kodakaraensis [95, 96]. Most other Themococci-specific proteins are of unknown function, although in a few cases limited similarity to domains in known protein families have been noted. A number of proteins (viz. PAB0643–PAB0644.1n; PAB1821–PAB1826) are clustered together in the P. abyssi genome, and it is possible that they may form functional units and are involved in related functions.
Proteins that are specific for Halobacteria
Extreme halophiles constitute another major class within Euryarchaeota. They require 5–10 times the salinity of seawater (ca. 3–5 M NaCl) for optimal growth [17, 97]. In order to grow in such high salinity environments, they have developed a set of physiological adaptation, such as: high internal concentration of potassium chloride, acidic proteome with low pI value, high GC content with GC bias in the wobble position, unique chloride pumps to maintain osmotic balance, etc. [17, 98, 99]. Among archaea, halobacteria also have the unique ability to use solar energy to generate a proton gradient to synthesize ATP. So far, the Class Halobacteria harbors one family with 15 genera and 4 species have been completely sequenced, including Halobacterium sp. NRC-1, Haloarcula marismortui, H. walsbyi and Natronomonas pharaonis [54, 98, 100, 101]. By performing blast searches on each protein in the Halobacterium sp. NRC-1 genome, we have identified 127 proteins, which are only present in all 4 Halobacteria species with only 3 exceptions (see Additional file 5).
Of the proteins listed in this Table, VNG0016H, VNG1096H, VNG2414H and VNG2563H are annotated as DNA-binding proteins or regulators because of the presence of HTH domain, but their exact functions have not been reported. VNG0667G is an ATP-binding protein of ABC transporter family. Several other proteins, such as VNG2089H and VNG2628H, have also been assigned possible functions based on weak similarity to known conserved domains in the CDD database , but their exact functions remain to be determined. Because of their high degree of conservation and uniqueness to halobacteria, the genes for these proteins likely evolved in a common ancestor of Halobacteria (Fig. 4) and they are presumably involved in unique physiological functions related to their adaptation to the hypersaline environment. Because of their specificity for Halobacteria, these proteins provide useful biomarkers for this group of species.
In addition to these proteins that are specific to all sequenced halobacterial species, we have also identified a large number of proteins either uniquely shared by 3 halobacterial species or only found in 2 halobacterial species (see Additional files 6 and 7). Surprisingly, these proteins are present in different combinations of halobacterial species. The four-halobacterial species are from 4 different genera within the Halobacteriales order and their relationships are unclear at present. The largest numbers of these proteins (i.e. 56) are uniquely shared by the Haloarcula, Haloquadratum and Natronomonas species, followed by 49 proteins that are restricted to Haloquadratum and Haloarcula. These results suggest that of these three species, Haloquadratum and Haloarcula are more closely related to each other and that Halobacterium might be the deepest branching of the four available halobacterial species (Fig. 4). However, the genome size of these halobacterial species varies and some of these protein sequences are present on plasmids found in these species, which makes it difficult to reliably infer their relationships solely based on the number of shared proteins. Among the proteins that are specific for halobacteria, only few have been assigned possible functions. Protein VNG2178H is annotated as PhiH1-like repressor and VNG0584H is assigned as a Rieske Fe-S protein. Two additional proteins VNG1720H and VNG2562H have been annotated as iron-binding proteins because of their similarity with FhuD and TroA_a domains, respectively . All of the other proteins are of unknown function.
Proteins that are specific for Thermoplasmata
The Thermoplasmata group is comprised of cell wall-less archaea, which resemble the bacterial Mycoplasma species . Generally, they are thermoacidophilic, aerobic or facultative anaerobic, and are able to reduce sulfur to H2S under anaerobic conditions [19, 55]. To date, this class include three families-Thermoplasmaceae, Picrophilaceae, and Ferroplasmaceae, each represented by one genus [103, 104]. Three complete genomes from this class (T. acidophilum, T. volcanium and P. torridus) are available at present (see Table 1) [19, 55, 63] and Ferroplasma acidarmanus Fer1 genome is draft assembled and sequence information for this is also available in the NCBI database. Our analyses have uncovered 77 proteins that are uniquely present in all four species belonging to this class (see Additional file 8(a)) (Fig. 4). Most of these proteins are present in all four available genomes, but a few are missing in one or two species, which is probably due to gene loss. Besides, we have also identified 33 proteins, which are shared only by the two Thermoplasma species (see Additional file 8(b)) and 17 proteins unique to P. torridus and F. acidarmanus (see Additional file 8(c)). The latter proteins indicate that species from Picrophilaceae and Ferroplasmaceae families are more closely related to each other (Fig. 4). All of these proteins are of unknown or predicted functions.
Proteins restricted to several archaeal lineages or showing sporadic distribution
In addition to the above proteins that are restricted to specific lineages of archaea, we have also identified 63 proteins, which are shared by several archaeal groups (see Table 7). The distribution pattern of these proteins could provide useful insights concerning the phylogenetic relationship between different groups. However, their distribution patterns could also be explained by gene losses in specific lineages or LGT between particular groups. Table 7 shows many proteins that are uniquely shared by various methanogenic archaea, Archaeoglobus and Thermococci. The first 5 proteins in Table 7(a) (PAB0076, PAB0138, PAB0965, PAB1927 and PAB1994) are present in all of the Thermococci and most of the methanogens. Four of these proteins are also present in A. fulgidus. The next 13 proteins in this Table are also uniquely found in most of the Thermococci as well as a number of methanogens and also in many cases in A. fulgidus. In addition, 6 proteins listed in Table 7(b) are only found in various Thermococci and A. fulgidus. These results suggest a closer relationship between the methanogenic archaea, A. fulgidus and Thermococci within the Euryarchaeota lineage. In conjunction with our earlier inference that A. fulgidus forms an outgroup of the methanogenic archaea, these results suggest that the above three groups are related in the following manner: Thermococci → A. fulgidus → Methanogens.
Although the relationship suggested above is the most likely explanation for the observed results, we have also come across three proteins (VNG1263c, MMP11287 and VNG2408c) that are uniquely present in various Halobacteria, A. fulgidus and different methanogens. To account for their species distribution, one has to postulate that their genes have been selectively lost from the Thermococci. In addition, 9 proteins are only found in various Halobacteria as well as Methanosarcinales and Methanomicrobiales (Table 7(c)). Their distribution requires again either selective gene losses from other lineages or LGT from Halobacteria to these methanogens.
Our analyses have also uncovered 30 proteins that are uniquely shared by species from Thermoplasmata and Sulfolobus (see Table 7(d)). Among these proteins, 7 are present in all Thermoplasmata and Sulfolobus species for which sequence information is available, while the remainder are missing in 1 or more species. It has been reported that there has been much lateral gene transfer between T. acidophilum and S. solfataricus, both of which inhabit the same environment . However, the shared presence of these proteins in these two groups could also result from a unique shared ancestry of these thermo-acidophilic archaea.
Another 43 Archaea-specific proteins are sporadically present in different archaeal species (see Additional file 9). A number of proteins in this group are present in a limited number (between 3 to 6) of archaeal species belonging to different groups. There are 2 possible explanations that can account for their sporadic distribution: First, it is possible that some of these genes are the remnants of sequences that also originated in an ancestral lineage of Archaea but they have been selectively lost in many species because they are not required for growth. Second, the sporadic presence of these genes in a number of archaeal species can also be explained if some of these genes originally evolved in a particular group or species of archaea and then transferred to other archaea by LGT . However, in view of the observed specificity of these genes/proteins for archaea, the LGTs in these cases need to be selective and limited to within archaea.
Comparative analyses of sequenced archaeal genomes presented here have led to identification of large numbers of proteins that are distinctive characteristics of either all archaea or its different main groups. Based upon these proteins, all of the main groups within Archaea (e.g. Crenarchaeota, Euryarchaeota, Halobacteria, Thermococci, Thermoplasmata, Methanogens) and their subgroups can now be clearly distinguished in molecular terms. The species distribution of these signature proteins strongly suggests that their genes have evolved or originated at various stages in the evolution of archaea, but once evolved, they are indicated to be generally stably retained in various descendents of these lineages with minimal gene loss or LGTs. Based upon the species distributions of these proteins, the evolutionary stages where the genes for these proteins have likely evolved are shown in Fig. 4. The evolutionary relationships among archaea have thus far been mainly inferred on the basis of their branching in phylogenetic trees based on 16S rRNA and certain protein sequences [2, 7, 13, 23–25]. The results of our analyses although they support many inferences reached based on phylogenetic trees (viz. identification of all of the main clades in phylogenetic trees in molecular terms) (Fig. 1) [2, 7, 13, 23–25], they also differ from them in important regards. In particular, our results shed important light on certain phylogenetic relationships that were very puzzling or were not resolved based on earlier studies. Some of these novel inferences are discussed below.
In phylogenetic trees based on 16S rRNA and various proteins sequences, the methanogenic archaea form at least two distinct clusters (see Fig. 1) [13, 29, 34, 56, 106]. In addition, in many of these trees, M. kandleri branches distinctly from all other methanogenic archaea [13, 34, 48]. The methanogenic archaea in these trees are interspersed by other groups of non-methanogenic archaea such as Halobacteriales, Archaeoglobus, Thermoplasmatales and Thermococcales (see Fig. 1) [13, 34, 48]. This has led to important questions concerning the origin of methanogenesis i.e. whether it evolved only once and its absence in the intervening lineages [13, 29, 35, 76]. To account for these results, it has been suggested that methanogenesis evolved once in a common ancestor of the above groups, i.e. different methanogenic archaea, Halobacteriales, Archaeoglobus, Thermoplasmatales and also possibly Thermococcales, comprising virtually all euryarchaeota, but that the various genes involved in this process were subsequently lost from different groups except the methanogens [13, 29, 56]. This scenario, in essence, proposes that the common ancestor of different physiologically and metabolically distinct groups within euryarchaeota was a methanogen and this capability was independently lost in all other lineages.
In contrast to this proposal, our phylogenomics analyses have identified 31 proteins that are uniquely present in virtually all methanogens, as well as many proteins that are specifically shared by different subgroups of methanogens. Of these proteins only about 1/3 are indicated to be directly involved in methanogenesis and the cellular functions of others are presently not known. The unique presence of such large numbers of proteins by nearly all methanogens, but none of the above groups of archaea, strongly indicates that the genes for these proteins evolved in a common ancestor of various methanogens. These results strongly suggest that all methanogenic archaea form a mononphyletic lineage exclusive of all other groups of archaea (Fig. 4). Importantly, these studies have also identified 10 proteins that are uniquely shared by all methanogens as well as by A. fulgidus. In contrast, we have not come across any protein that various methanogenic archaea uniquely share with any of the Halobacterales or Thermoplasmatales. These observations are highly significant because they strongly suggest that Archaeoglobus and all of the methanogens shared a common ancestor exclusive of all other archaea. In other words, the ancestral lineage that led to the origin of methanogenesis very likely evolved from the Archaeoglobus lineage (Fig. 4). It is also significant that of the proteins that are uniquely shared by Archaeoglobus and methanogens, several form part of complexes that are important for nitrogen assimilation and methanogenesis. These results support the view that these characteristics have their origin within the Archaeoglobus lineage.
The present work also provides clarification regarding the phylogenetic position of M. kandleri. In phylogenetic trees based on 16S rRNA or different protein sequences, the branching of this species is highly variable [13, 34, 47, 48] and it often forms the deepest branch within the Euryarchaeota. In the present work, we have identified 31 proteins that are uniquely shared by all methanogens including M. kandleri, as well as 10 proteins that M. kandleri specifically shares with various Methanobacteriales and Methanococcales, and 15 additional proteins that are only found in M. kandleri and the two Methanobacteriales species (M. thermoautotrophicus and M. stadtmanae). These observations reliably place M. kandleri with other methanogenic archaea with the Methanobacteriales as its closest relatives (Fig. 4). Our results also suggest a closer relationship of the Thermococcales to the Archaeoglobus and methanogenic archaea, although this relationship is not as strongly supported as between Archaeoglobus and Methanogens.
The observed differences in the evolutionary relationships among methanogens based upon phylogenomics analyses versus those by traditional phylogenetic methods can in principle be accounted for by three explanations. First, it is possible that the branching patterns of various clades in phylogenetic trees are misleading and they have been affected by factors such as long branch attraction effect [107, 108]. Second, the polyphyletic branching of methanogens can also be explained (as indicated earlier) if the genes uniquely shared by all methanogens evolved in an early branching lineage such as M. kandleri, but subsequently they were either completely or partially lost from various non-methanogenic (viz. Halobacteriales, Thermoplasmatales and Archaeoglobus) groups that lie in between the two methanogenic clusters (Fig. 1). Third, lateral transfer of these genes from one methanogenic archaea to all others can also explain these results. Of these possibilities, we favour the first explanation, as the last two require extensive gene loss or LGT from (or into) multiple independent lineages.
The present work also supports the placement of N. equitans within the Euryarchaeota lineage. N. equitans has a very small genome (only 0.49 Mb), which is at least 3 times smaller than any other archaeal genome. Due to its very small size, there are only 6 genes that N. equitans uniquely shares with all other archaea. However, our analysis indicates that whereas N. equitans shares a few genes (PAB2404 and PAB 0188) with most of the Euryarchaeota, it does not share any gene uniquely with most of the Crenarchaeota species, indicating its closer affinity for the former lineage. Although our analysis of the N. equitans genome has not revealed any strong signals indicating its specific affinity for any of the Euryarchaeota groups, the shared presence of some proteins by N. equitans and Thermococci (and in some cases also A. fulgidus and methanogens) suggest that it may be related to the Thermococci. However, because of the extensive gene losses that have occurred in this genome, we are not able to draw any reliable inference in this regard. Therefore, although we have depicted N. equitans as a deep branching lineage within Euryarchaeota (Fig. 4), based upon our analysis, its placement within Euryarchaeota is not resolved.
The present work also suggests that Thermoplasmatales might be a deeper branching lineage within Euryarchaeota in comparison to the Thermococcales, Halobacteriales, Archaoglobous and Methanogens. This inference is suggested by the observation that a number of proteins that are uniquely present in almost all other Euryarcheota species are missing in the Thermoplasmatales. Although the absence of these proteins in the Thermoplasmatales can be explained by specific gene loss, the possibility that the genes for at least some of these proteins have evolved after the branching of Thermoplasmatales deserves serious consideration. The deeper branching of the Thermoplasmatales within the Euryarchaeota will place it closer to the Crenarchaeota. Such a placement could prove helpful in understanding why so many genes (i.e. 30) are uniquely shared by various Thermoplasmatales and the Sulfolobales.
For the archaeal-specific proteins identified in the present work, sequence information at present is available from only a limited number of archaeal species. Hence, it is important to obtain information for these genes/proteins from other archaeal species to confirm whether these proteins are distinctive characteristics of the specified groups or a subgroup of such species. These proteins in addition to their utility for phylogenetic and taxonomic studies also provide valuable means for understanding archaeal biology [35, 38]. The cellular functions of most of these proteins are not known and further studies in this regard should prove very helpful in the discovery of novel biochemical and physiological characteristics that are unique to either all or different groups of archaea . Lastly, the primary sequences of many of these genes/proteins are also highly conserved and they provide novel means for identification of different groups of archaea in various environmental settings by means of PCR amplification and other molecular biological and immunological methods.
Identification of Archaea-specific proteins
To identify proteins which are specific for Archaea or its various subgroups, all proteins in the genomes of A. pernix K1 (APE), S. acidocaldarius DSM 639 (Saci), P. aerophilum str. IM2 (PAE), P. abyssi GE5 (PAB), M. maripaludis S2 (MMP), M. kandleri AV19 (MK), M. burtonii DSM 6242 (Mbu), Halobacterium sp. NRC-1 (VNG), H. walsbyi DSM 16790 (HQ), T. acidophilum DSM 1728 (Ta) and P. torridus DSM 9790 (PTO), were analyzed. Protein-protein blast searches were carried out on each individual protein using the default parameters, without the low complexity filter, to identify different proteins where all significant hits were from archaea . The results of blast searches were inspected for sudden increase in Expected values (E-values) from the last archaeal species in the search to the first non-archaeal organism. The proteins that were of interest generally involved a large increase in E-values from the last archaeal hit to the first hit from any other organism. Further, the E values of these latter hits were expected to be in a range higher than 10-4, which indicates a weak level of similarity that could occur by chance. However, higher E-values are sometimes acceptable for smaller proteins as the magnitude of the E-value depends upon the length of the query sequence.
All promising proteins identified by the above criteria were further analyzed using the position-specific iterated (PSI) blast program. In the present work, a protein was considered to be archaeal-specific if all hits producing significant alignments were from the indicated groups of archaeal species. However, we have also retained a few proteins where 1 or 2 isolated species from other groups (e.g. bacteria or eukaryotes) also had acceptable E-values. We consider these proteins to be also archaea-specific and their presence in isolated unrelated species is very likely due to lateral gene transfer. For all archaea-specific proteins described here, the protein ID, accession number and their possible functions (also COG or CDD number [102, 110]) are presented in Tables 2, 3, 4, 5, 6, 7, 8 and Additional files 1, 2, 3, 4, 5, 6, 7, 8, 9. All proteins indicated in various tables are specific for the Archaea based on these criteria unless otherwise mentioned.
Phylogenetic analyses was carried out on a concatenated sequence alignment of 31 universally distributed proteins . The information regarding these proteins is provided in the Additional file 10. For each of these proteins sequences from all 29 archaeal species were downloaded and multiple sequence alignments were created using ClustalX 1.83 program. A concatenated sequence alignment for all 31 proteins was imported into Gblocks 0.91b  to remove poorly aligned region. The resulting final alignment of 6,252 amino acid sites was used for phylogenetic analyses. A NJ tree based on this dataset was constructed by TREECON 1.3b program with Kimura two-parameter model distance ; Maximum-Likelihood tree were computed under a WAG+F model plus a gamma distribution with four categories by TREE-PUZZLE 5.2 [113, 114]; Maximum-Parsimony tree were obtained by Mega 3.1 package . All of the trees were bootstrapped 100 times.
We thank Inas Radhi, Amy Mok, and Gayathri Vaidyanathan for assistance in carrying out blast searches on some of the archaeal genomes. We also thank Venus Wong for computer support that facilitated the blastp analyses. This work was supported by a research grant from the National Science and Engineering Research Council of Canada.
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