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Archaea. 2006 August; 2(1): 11–30. Published online 2006 January 23. | PMCID: PMC2685588 |
Copyright © 2006 Heron Publishing—Victoria, Canada Distribution, structure and diversity of “bacterial” genes encoding two-component proteins in the Euryarchaeota Mark K. Ashby*1,2 1 Department of Basic Medical Sciences, Biochemistry Section, University of the West Indies, Mona Campus, Kingston 7, Jamaica 2 School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, U.K. Received June 13, 2005; Accepted January 12, 2006.
The publicly available annotated archaeal genome sequences (23
complete and three partial annotations, October 2005) were searched
for the presence of potential two-component open reading frames (ORFs)
using gene category lists and BLASTP. A total of 489 potential
two-component genes were identified from the gene category lists and
BLASTP. Two-component genes were found in 14 of the 21 Euryarchaeal
sequences (October 2005) and in neither the Crenarchaeota nor the
Nanoarchaeota. A total of 20 predicted protein domains were identified
in the putative two-component ORFs that, in addition to the histidine
kinase and receiver domains, also includes sensor and signalling
domains. The detailed structure of these putative proteins is shown,
as is the distribution of each class of two-component genes in each
species. Potential members of orthologous groups have been identified,
as have any potential operons containing two or more two-component
genes. The number of two-component genes in those Euryarchaeal species
which have them seems to be linked more to lifestyle and habitat than
to genome complexity, with most examples being found in
Methanospirillum hungatei, Haloarcula
marismortui, Methanococcoides burtonii and
the mesophilic Methanosarcinales group. The large numbers of
two-component genes in these species may reflect a greater requirement
for internal regulation. Phylogenetic analysis of orthologous groups
of five different protein classes, three probably involved in
regulating taxis, suggests that most of these ORFs have been inherited
vertically from an ancestral Euryarchaeal species and point to a
limited number of key horizontal gene transfer events.
Keywords: histidine kinase, hybrid kinase, response regulator
Two-component systems are one of the key means by which bacteria respond
to environmental changes ( Hoch
2000, Stock et al. 2000,
Alves and Savageau 2003,
Hellingwerf 2005). They are
assumed to be of bacterial origin, having radiated into archaea and some
eukaryotes by horizontal gene transfer (HGT)
( Koretke et al. 2000).
Two-component systems consist of a sensor and a response protein. The
sensor protein is characterized by a histidine kinase (HK) made up of
two main domains, a phosphoacceptor (HisKA) and a histidine kinase
ATPase (HATPase) and, in many cases, other sensory domains are present
( Galperin et al. 2001,
Zhulin et al. 2003). The response
protein (response-regulator, RR) is characterized by a response
regulator domain that has a conserved aspartate residue. The histidine
kinase autophosphorylates a conserved histidine residue in response to a
signal and the phosphate group is then transferred to the conserved
aspartate residue of the response-regulator. The transfer of the
phosphate group to the response-regulator elicits a response causing a
change in taxis, development or gene expression. Histidine kinases and
response-regulators are sometimes found together in a single polypeptide
known as a hybrid kinase ( Hoch
2000, Stock et al. 2000).
The recognition of the Archaea as a distinct division of life has been
strengthened by the availability of a number of complete genome
sequences, representing three phyla (Euryarchaota, Crenarchaeota and
Nanoarchaeota). This has, in turn, enabled a more rigorous phylogenetic
analysis based on the fusion of ribosomal protein sequences
( Matte-Tailliez et al. 2002,
Brochier et al. 2004,
Bapteste et al. 2005,
Makarova and Koonin 2005) and
clusters of conserved orthologous genes (COGs)
( Makarova and Koonin 2003).
Analysis of genome sequences has revealed genes of bacterial origin in
the genomes of archaea and vice versa
( Nelson et al. 1999). The
importance of HGT in the evolution of prokaryotes and the implications
for phylogeny and definition of species is still being discussed
( Ochman et al. 2000,
Forterre et al. 2002,
Boucher et al. 2003,
Koonin 2003,
Kurland et al. 2003,
Lawrence and Hendrickson 2003).
For bacteria, it has been shown that the number of two-component genes
possessed by an organism is related to the complexity of its genome, its
physiology and the changeability of its habitat
( Ashby 2004,
Galperin 2005). The greater the
value of any of those parameters, the greater the need for regulation of
cellular activities.
The aim of this study was to analyze the complement of genes in archaeal
genomes that could encode two-component proteins. The putative
two-component proteins were classified by their domain structure, and
the number of each class was determined for each species. Potential
orthologous groups and those that may be part of operons, with two or
more two-component genes, are indicated. Phylogenetic analysis of
possible orthologous groups representing five classes of protein, three
associated with taxis, is shown.
Genome sequence data
The list of publicly available Euryarchaeal genome sequences is shown
in Table 1, along with brief
details of the habitat, physiology, genome size, putative number of
open reading frames (ORFs) and the abbreviation used with gene
sequences ( Makarova and Koonin
2003). The sequences and annotations for the annotated
sequences (up to October 2005) were accessed at the Integrated
Microbial Genomes (IMG) server
( http://img.jgi.doe.gov/pub/main.cgi)
and HaloLex
( http://
www.halolex.mpg.de/). The identity of potential two
component genes was determined by reference to the published
assignments located at
http://www.tigr.org/tdb/
( Bult et al. 1996,
Smith et al. 1997,
Kawarabayasi et al. 1998,
Klenk et al. 1997,
Ng et al. 2000,
Deppenmeier et al. 2002,
Slesarev et al. 2002,
Galagan et al. 2002,
Cohen et al. 2003,
Baliga et al. 2004,
Falb et al. 2005). This was
supplemented by BLASTP ( Altschul et al.
1997) searches of each genome with a battery of two component
domains (domains used include receivers from CheY and OmpR,
HisKA/HATPase and Hpt; see Table A1) from Methanosarcina
acetivorans and E. coli K12 at IMG
( http://img.jgi.doe.gov/pub/main.cgi),
The Integrated Genome Resource (TIGR,
http://www.tigr.org/tdb/)
or the National Center for Biotechnology Information (NCBI,
http://www.ncbi.nlm.nih.gov/).
| Table 1.
Strain description of members of the Euryarchaea for which there
are publicly available genome sequences as of October 2005. The
gene name prefix is used with the gene designations to aid in
(more ...) |
Bioinformatic analysis
Putative two-component domains were initially assigned in ORFs by Pfam
batch analysis
( http://www.sanger.ac.uk/Software/Pfam/;
Bateman et al. 2004). Domains
were recorded for each two-component gene only if they were scored as
“Pfam’s trusted match thresholds.” Domain
assignments were checked and modified using the more extensive domain
assignments at InterPro
( http://www.ebi.ac.uk/interpro/).
The results were used to classify the putative two-component proteins
by domain organization using a nomenclature adapted from
Ohmori et al. (2001), with each
group subdivided by the organization of the identified signalling
domains. The cartoon style diagrams that present the domain
organization of the deduced sequences were constructed from these
data, with the sizes of the domains roughly in proportion to each
other. For clarity, each gene name begins with a four character
acronym (except for Haloarcula marismortui,
Pyrococcus abyssi GE5 and Pyrococcus
horikoshii OT3, see Table
1) followed by either the locus tag that can be found at IMG or
HaloLex
( http://img.jgi.doe.gov/pub/main.cgi
and
http://www.halolex.mpg.de/)
or the gene object identifier if the sequencing or annotation is
incomplete.
To determine orthologous groups, orthology information, based on the
bidirectional best hits from BLASTPs of each organism against each
other organism polypeptide, is accessible at IMG
( http://img.jgi.doe.gov/pub/main.cgi).
This definition is not completely accurate, but it provides a useful
approximation as it is not always possible to know whether the
polypeptides arose from a single gene present in the last common
ancestor (orthologues) or from a gene duplication within a genome
(paralogues). Alignments for phylogenetic analysis were performed by
TCoffee ( Notredame et al. 2000)
and accessed at the Centre Nationale de la Recherche Scientifique
website
( http://igs-server.cnrs-mrs.fr/Tcoffee/tcoffee_cgi/index.cgi)
and ClustalW alignments ( Thompson et
al. 1994) were performed at the European Bioinformatics
Institute
( http://www.ebi.ac.uk/clustalw/).
Representatives from three bacterial phyla were included in the
alignments (chosen by having the best match to one of the archaeal
ORFs, either as an orthologue or by BLASTP at IMG). Phylogenetic
analysis by neighbor-joining (Bootstrap 250) was performed using MEGA
version 3.0 ( Kumar et al. 2004)
and by maximum-likelihood ( Felsenstein
1996) using Molphy, accessed at the Institut Pasteur,
biological software website
( http://bioweb.pasteur.fr/intro-uk.html#phylo).
The structural classification of potential two-component proteins is
shown in Table 2. No
two-component encoding gene could be found in the Crenarchaeota or
Nanoarchaeota (data not shown). Sensor domains are drawn as ellipses and
two-component (HisKA, HATPase_c and response regulator) and output
domains are drawn as rectangles. parentheses followed by figures
indicate the number of similar domains that may be found in the proteins
listed in each subclass.
| Table 2.
Compilation and cartoon diagrams of all putative archaeal open
reading frames encoding two-component proteins. Abbreviations;
Cach = Cache; ConA = ConA-like glucanase; Gly = Glycos_transf_2;
HKA (more ...) |
Histidine kinases
Different types of histidine kinases (HK) are listed in
Table 2A. Histidine kinases
contain two domains; a dimerization and a phosphoacceptor domain
(HisKA or HisKA_2) and a HATPase_c domain
( Grebe and Stock 1999). HisKA
and HisKA_2 are part of a His kinase A phosphoacceptor domain
superfamily that also includes HWE_HK and HisKA_3
( Karniol and Vierstra 2004;
Pfam accession CL0025).
HKI
Histidine kinase Is are HKs containing HisKA and HATPase domains.
There may be other domains in some of these examples which are not
currently recognized. The HKI ORFs vary greatly in size, ranging
from 175 to 592 amino acids in length.
HKII
Histidine kinase IIs are HKs containing sensor GAF and PAS/PAC
domains. The GAF domains (c GMP
phosphodiesterase, adenylyl cyclases,
bacterial transcription factors FhlA) are
associated with small molecule binding, in particular cAMP and cGMP
( Aravind and Ponting 1997,
Ho et al. 2000,
Anantharaman et al. 2001). The
GAF domain is usually found in combination with PAS
( Drosophila period clock
protein, vertebrate aryl hydrocarbon receptor
nuclear translocator and Drosophila
single-minded protein) or PAC
( PAS- associated
C-terminal motif) domain, or both. One class
of PAS domains is known to bind cofactors such as heme and FAD
( Bibikov et al. 2000,
Sardiwal et al. 2005).
Sensing of light, oxygen or redox potential by PAS domains requires
cofactors, whereas sensing signals such as voltage, xenobiotics and
nitrogen availability does not
( Ponting and Aravind 1997,
Gilles-Gonzalez and Gonzalez
2004). The PAC domains are proposed to contribute to the PAS
domain fold. The shared feature of GAF and PAS/PAC domains is the
binding of a diverse set of regulatory small molecules that often
remain unidentified; all three domains are common signal
transduction system components
( Anantharaman and Aravind
2001, Zhulin et al.
2003). There is one example containing Cache and one
containing SBP_bac_3 (bacterial extracellular solute-binding
proteins, family 3). The Cache domain is a signalling domain found
in animal calcium channel subunits and it is thought to form an
extracellular or periplasmic ligand sensor
( Anantharaman and Aravind
2001). SBP_bac_3 is involved in active transport of solutes
across the cytoplasic membrane and in the initiation of signal
transduction pathways ( Tam and Saier
1994). This is by far the largest subgroup of ORFs,
containing 161 out of the total of 489 (33% of the total).
HKIII
Histidine kinase IIIs are HKs that possess a HAMP
“linker” ( histidine kinase,
adenylyl cyclase,
methyl-accepting chemotaxis protein and
phosphatase) domain. The HAMP domain is
usually associated with the transmission of a signal across a
membrane from periplasmic ligand-binding domains
( Aravind and Ponting 1999,
Appleman and Stewart 2003,
Zhu and Inouye 2004). Eight
examples of HKIIIs have an N-terminal putative periplasmic
signalling CHASE4 domain and four have an N-terminal periplasmic
signalling Cache domain ( Anantharaman
and Aravind 2001, Zhulin et
al. 2003). These domains are positioned next to the HAMP
domain, presumably for efficient transfer of the signal.
HKVI
Histidine kinase IVs are the CheA-like chemotaxis signalling
proteins that contain an N-terminal Hpt
( histidine
phospho transfer) and
Hkd ( histidine kinase
dimerization) domain and a C-terminal CheW
domain. Some contain one or two P2 domains between the Hpt and Hkd.
The Hpt domain is involved in mediating phosphotransfer from one
receiver domain to another ( Hoch
2000). Hkd (H-kinase-dim) is the dimerization domain of CheA
and CheW that interacts with methyl-accepting chemotaxis proteins
(MCPs), relaying signals to CheY, and thereby affecting flagellar
rotation ( West et al. 1995).
The P2 domain is involved in enhancing the interaction of CheY with
the HK ( Jahreis et al. 2004,
Stewart and van Bruggen
2004). Thermococcus kodakaraensis has two
open reading frames with a frame shift mutation that probably
encodes for a CheA-like protein. All of the HKVI genes discussed are
located close to other genes that could be involved with signal
transduction and are probably transcribed as single operons (see
Table A2).
HATPase_c
These contain no dimerization or phosphoacceptor domains currently
recognized at INTERPRO.
His_KA
There are five groupings that contain His_KA without a discernable
HATPase_c domain.
Response regulators
Response regulators (RR) are listed in
Table 2B. These contain a
characteristic receiver (RR/T_reg) domain, which is about 120 amino
acids long and contains a conserved aspartate residue about halfway
along the molecule that accepts a phosphate group from an HK.
RR I
Response regulator Is are simple orphan (no other domain detected)
RRs, representing the second largest group of two-component ORFs
(24% of the total).
RRIII
Response regulator IIs contain an RR fused to a potential DNA
binding domain. Such regulators are found only in H.
marismortui. Of these, there are only three examples that
containeither the HTH_10 or DUF24 domain (PF04967
and PF 01638). These are the only RRs that are possibly
transcriptional regulators, but there may be other currently
unidentified DNA-binding domains in other RRs or hybrid kinases.
RRIV
Response regulator IVs contain an N-terminal RR fused to output or
signal domains. There are 16 examples of CheB fused to the RR. The
CheB domain is related to methylesterase and is likely to be
concerned with chemotaxis ( West et
al. 1995). There is one example of two RRs fused to a
glycosyl transferase domain in M.
thermoautotrophicus (Pfam Accession number: PF00353). The
glycosyl transferase domain is involved in transferring sugar
moieties from a donor to recipient molecules. There are a lot of
Methanospirilum hungatei ORFs fused with PAS/PAC or
GAF domains, or both, however, as the annotation is incomplete, some
of these ORFs may turn out to be part of hybrid kinases.
Hybrid kinases
Hybrid kinases (HY) are shown in Table
2C. They are defined as containing both HK and RR domains. The
nomenclature is based on the position and number of RR with respect to
the HK. There is an incomplete HYI in A. fulgidus
that has a PAC/ PAS and GAF sensor domain, but no discernable HATPase
domain.
HYI
Hybrid kinase Is have a single RR N-terminal to the HK.
HYII
Hybrid kinase IIs have a single RR C-terminal to the HK. There is
only one example in M. acetivorans.
HYIII
Hybrid kinase IIIs have two RRs either N or C-terminal to the HK.
Distribution of putative two-component ORFs
The total number of ORFs within each class of two-component proteins,
for each species of Euryarchaeota, is shown in
Table 3. No two-component ORFs
were found in the four Crenarchaeota species or N. equitans
(data not shown). No two-component ORF was found in
M. jannaschii, M. kandleri,
P. furiosus or in any of the members of the
Thermoplasmales. The three other Pyrococcus species
each have only three two-component ORFs ( Thermococcus
kodakaraensis HKVI that has a frame shift Tkod_61070420/30,
that could be a sequencing error has been counted as one),
representing 0.17% of the protein-coding capacity of the genome.
Methanococcus maripaludis and Halobacterium
also have a small number, six (0.34%) and 16 (0.64%),
respectively. Archaeoglobus fulgidus, M.
thermoautotrophicus and the four Methanosarcinales groups
have a comparatively large number of two-component ORFs, from 23 to
67. This represents from 1.03 to 1.48% of the coding capacity of the
four complete genome assignments. Haloarculamarismortui has the largest number of two-component
encoding genes, of the complete annotations, which represents 1.93% of
the total protein coding capacity of the genome.
Methanospirillum hungatei appears to have the largest
number of two-component genes at 87, though the annotation of the
genome is incomplete (so no percentage is given in
Table 3). The HKs form half to
two-thirds of the two-component ORFs for each species (except
Pyrococcus sp. and Methanospirillum
hungatei). The DNA-binding domains (putative) were only
detected as part of the RRs in H.marismortui.
| Table 3.
Distribution of euryarchaeal two-component open reading frames.
The total number of identified two-component genes are shown
(Total 2-C) and are given as a percentage of the total protein
(more ...) |
The PAS/PAC and GAF sensory domains are found in 293 of the 489
putative proteins surveyed. These sensory domains are absent in the
Pyrococcus sp. A total of 18 ORFs were found that
contain the HAMP domain that would in most cases be involved in
transferring signals from sensor domains detecting information outside
the cell.
Orthologous groups
Potential orthologous groups are shown in
Table 4. These results are
based on the bidirectional best hits from BLASTPs at IMG. The
identification of orthologous groups at IMG may not be correct in all
cases as some groupings may include ORFs that are due to gene
duplication, hence a paralogue (in a different organism) rather than
an orthologue. It is, nevertheless, a useful tool for assigning
putative orthologous groups when no functional information is
available. The groups have been named with a three letter acronym for
ease of reference ( Table 4). In
arr18/19, RRIV-CheB, the grouping was modified from
the information at IMG based on the phylogenetic analysis presented in
(see below). There are
many orthologous groups that contain two or three members,
particularly within the Methanosarcinales. The more interesting groups
are those that have more members or that have members in different
genera. These will be discussed below, particularly those that are
part of taxis operons ( ahk40–43 , arr7,
arr10, arr18 and arr19).
| Table 4.
Potential orthologous two-component open reading frames.
|
Phylogenetic analysis
to 5 show
neighbor-joining and the supplementary Figures A1 to A5 contain the
maximum likelihood phylogenetic analyses of alignments from TCoffee
analysis. Phylogenetic analysis of the same ORFs was also performed on
alignments made by ClustalW (data not shown), but the results were not
found to differ significantly. Figure 7 contains the ORFs from the two
HKII groups, ahk5 and ahk22, with
the three closest bacterial ORFs (to MaceMA2890) from Cyanobacteria,
Firmicutes and Proteobacteria. Figure 8 is composed of ORFs from the
four HKVI ‘CheA like’ groups,
ahk40–43, and the three
closest bacterial ORFs (to MaceMA0014) from Thermatogae, Firmicutes
and Proteobacteria. is
the analysis of a number of RRI orphans, arr7 and
arr10 (from putative taxis operons),
arr12 and arr14 (> 200 amino
acids) with bacterial ORFs from Thermatogae, Firmicutes and
Proteobacteria (closest to MaceMA3068).
shows the results for
the two RRIV CheB orthologous groups from taxis operons,
arr18 and arr19 with bacterial
representatives from Thermatogae, Proteobacteria and Actinobacteria
(closest to MaceMA0015).
shows results for ahy2 and bacterial representatives
from Cyanobacteria, Actinobacteria and Proteobacteria.
Linked genes
Genes that are located close to each other on the genome and
transcribed in the same orientation are shown in Table A2. Most of
these are likely to be part of operons. This provides clues to some
cognate pairs of HKs, HYs and RRs. All putative HKVI encoding genes
are located with other “chemotaxis” genes in
“chemotaxis operons,” including two such operons for
M. acetivorans and M. mazei.
Included in these “chemotaxis operons” are the orthologous
groups, ahk40–43 , arr7, arr10
and arr18 and arr19
( Table 4).
Distribution of two-component ORFs
Ten species, representing four genera have at least 17 putative
two-component ORFs. Some of these two-component ORFs are quite
sophisticated in structure, including the multiple sensor HKIIs,
CheA-like HKVIs and the hybrid kinases. The results presented here
show that a number of euryarchaeal species have an extensive array of
two-component sensory ORFs. These proteins may sense a number of
different internal signals by means of PAS/PAC domains and their
associated cofactors ( Ponting and
Aravind 1997, Gilles-Gonzalez
and Gonzalez 2004). In addition, the potential to sense other
small molecules (particularl cNMPs) via the GAF domains
( Aravind and Ponting 1997,
Ho et al. 2000,
Anantharaman et al. 2001) and
extracellular signals, by the CHASE4 and Cache putative sensory
domains, via HAMP domains ( Anantharaman
and Aravind 2001, Zhulin at al. 2003) shows that these
organisms (in particular H.marismortui,
Natronomonas pharaonis, Methanospirillum hungatei and the
Methanosarcinales) possess sophisticated and complex sensory networks.
As yet, none of these putative two-component genes have a functional
name, so functions can be assigned only by similarity. The DNA-binding
RRs are common in bacteria that regulate gene expression
( Ashby 2004,
Galperin 2005). However only
three RRs have been identified with putative DNA binding domains, all
in H. marismortui. If regular indiscriminate HGT were
taking place, one would expect to see more DNA-binding RRs in archaeal
sequences. Presumably the large number of orphan RRs are involved in
regulation of cellular activity by interacting directly with other
proteins. Transcriptional control is probably maintained by the many
DNA-binding domains that have been identified as part of one-component
systems in archaea ( Ulrich et al.
2005). In these systems the DNA-binding output domain is linked
directly to a sensor domain without any phosphotransfer.
Of the species that have the most two-component genes, H.
marismortui and Natronomonas pharaonis are
halophilic and the Methanosarcinales and Methanospirillum
hungatei are mesophiles. The mesophiles coexist with a large
and diverse population of bacteria, giving ample opportunity for HGT,
whereas the opportunity for HGT in the halophilic organisms would be
more restricted. This begs the question of how the distribution of
two-component genes that can be seen in the Euryarchaeota arose. Was
it through HGT exclusively or by vertical transfer from a common
ancestral euryarchaeal organism coupled with gene duplications?
Phylogeny and inheritance of two-component ORFs
For ahk5 and ahk22, shown in
, the phylogeny of each
group agrees with the current phylogeny of these organisms and the
position of the three bacterial examples indicates that the two groups
may have arisen through a separate HGT event in an ancestral
euryarchaeal species for ahk5 and possibly, into an
ancestral methanogen for ahk22.
The results for the CheA-like HKVI ORFs are shown in Figure 8.
Ahk40, ahk42 and
ahk43 (except Mhun_401793120) cluster together and
probably represent vertical inheritance from a single HGT event into
an ancestral Euryarchaeota species (one bacterial ORF from T.
maritima giving the best match). Ahk41
appears to be a separate group, found in the Methanosarcinales, that
clusters on its own and seems to be more closely associated with the
Firmicutes and Proteobacterial examples, presumably representing a
separate HGT event. The three Methanospirillum
hungatei ORFs seem to be due to separate (Mhun_401793120
probably should not be in ahk43) HGT events and
Mhun_401784470 and Mhun_401776240 are probably true paralogues.
shows the results for
four orphan RR groups. The two groups, associated with putative taxis
operons ahk7 and ahk10, group
closely together, however, ahk10, which is found only
in the Methanosarcinales is probably due to an HGT event into a direct
ancestor of this group. The other two orthologous groups,
arr12 and arr14 are quite separate
from the first two mentioned groups (arr7 and
arr10) and probably arose from separate HGT events
into the ancestors of methanogens (AfulAF2419 appears to be a distant
member of ahk12).
shows the results for
the two RRIV-CheB orthologous groups associated with taxis. The
arr18 orthologous group found in Methanosarcinales
groups separately from arr19, being closer to two of
the bacterial ORFs. Therefore arr18 appears to be the
result of a separate HGT event in an ancestor of the
Methanosarcinales, whereas arr19 appears to be the
result of an HGT event into an ancestor of Euryarchaeota.
The phylogeny for ahy2 (the biggest hybrid kinase
orthologous group), shows that these members probably arose from more
than one HGT event. The combined results for the orthologous groups
found in potential taxis operons are shown in Table A2.
The operon that contains HKVI
(ahk40/42/43), RRI
(arr7) and RRIV-CheB (arr19) appears
to have arisen as an HGT event that transferred the whole operon into
an ancestor of the Euryarchaeota. In contrast, the taxis operon
containing HKVI (ahk41), RRI (arr10)
and RRIV-CheB (arr18) appears to have arisen from a
separate HGT event of the whole operon into a direct ancestor of the
Methanosarcinales.
The results presented here suggest that HGT has taken place from
bacterial species both into ancestral Euryarchaeota and more recently
into the methanogens. However the large numbers of two-component genes
in the mesophilic methanogens and the Halobacteriales probably reflect
their well known metabolic flexibility
( Bapteste et al. 2005,
Falb et al. 2005). This in
turn, necessitates an increased requirement for regulation of cellular
activity in a changing environment rather than the increased potential
for HGT from bacteria. Most of the two-component ORFs that can be
observed in these groups of organisms are probably derived from
paralogous gene duplication events, the number of two-component ORFs
observed would be driven by the requirement to control cellular
activity as the organisms evolve. A limited number of HGT events could
be sufficient to account for the diversity of phosphotransfer and
sensory domains.
Any function of two-component ORFs is inferred by homology to known
bacterial genes (e.g. HKVI and chemotaxis) and awaits in situ or in
vitro studies, or both. This highlights the importance of interfacing
between bioinformaticians and biochemists to plan experiments in an
informed way, particularly where orthologues are identified and found
in more than one genus and hence may play central roles in cellular
regulation.
Mark Ashby was supported by New Initiative Funding from the University
of the West Indies. The author wishes to thank John Allen, Elke
Dittmann, Conrad Mullineaux and Ruth-Sarah Rose for critical reading of
this manuscript.
Table A1.
Two-component protein domains from M.
acetovrans (M. ace) and
Escherichia coli K12 (E. coli)
used for BLASTP searches, showing the online accession numbers
and the amino acid range that was used. Abbreviation: aa = amino
acids.
| Domain | Species | Gene | Amino acid region |
| | CheY Receiver | E. coli | NP_416396.1 | | | M. ace | MA0016 | | | M. ace | MA3068 | | | OmpR Receiver | E. coli | NP_417864.1 | aa 6–124 | | Histidine kinase | E. coli | NP_417863.1 | aa 234–439 | | M. ace | MA0490 (HisKA_2) | aa 639–847 | | Hpt | E. coli | NP_415513.1 | aa 815–896 | | M. ace | NP_614988 | aa 5–106 |
Table A2.
Closely linked genes that may be part of operons.
| Assigned gene no. | Classification | Orthologue number | Additional information |
| | Archaeoglobus fulgidus | | | | | AF448 | His_KA PACPASGAF | | | | AF449 | RRI-CheY | | | | AF450 | HKIII + 1 PASPAC | | | | AF1042 | RRI-CheY | arr7 | AF1055 mcp | | AF1041 | RRIV-CheB | arr18 | AF1044CheW | | AF1040 | HKVI | arr40 | AF1039 CheC | | AF1472 | HYI-HisKA | ahy2 | | | AF1473 | RRI-CheY | arr9 | | | AF2419 | RRI-CheY | arr12 | | | AF2420 | His_KA PACPASGAF | | | | | | | | Halobacterium | | | | | VNG0974G | RRI-CheY | arr7 | VNG0976G CheW | | VNG0973G | RRIV-CheB | arr19 | VNG0970G CheC1 VNG0971G | | HKVI | ahk43 | VNG0967G CheD | | | VNG0966G CheR | HKIII | ahk22 | | | VNG1374G | HATPase HAMP | | | | VNG1375G | | | | | VNG2036C | RRI-CheY | arr1 | | | VNG2037C | HKII | | | | | | | | Haloarcula marismortui | | | | | rrnAC0410 | HKII + 2PASPAC | arr9 | | | rrnAC0411 | RRI-CheY | | | | rrnAC0412 | HYI | | | | rrnAC0413 | HKII + 1PASPAC | | | | rrnAC0456 | HATPase_c+ gyra | | Top6B | | rrnAC0457 | HATPase_c | | Top6A | | rrnAC2204 | RRIV-CheB | arr19 | rrnAC2206 CheR | | rrnAC2205 | HKVICheW-CheA | ahk43 | | | rrnAC2692 | HYI + PASPACGAF | | | | rrnAC2694 | HATPase_c + PAS | | | | | | | | Methanobacter thermoautotrophicus | | | | | MTH444 | HKI | ahy9 | | | MTH445 | RRI-CheY | arr9 | | | MTH446 | HYI + (PASPAC)2 | ahy2 | | | MTH447 | RRI-CheY | arr6 | | | MTH457 | RRIV-PACPAS | | | | MTH459 | HKI | | | | MTH548 | RRIV-G_transf | | | | MTH549 | RRI-CheY | | | | MTH901 | HYI | | | | MTH902 | HYI-PASPAC | | | | | | | | Methanococcus maripaludis | | | | | MMP0926 | RRI-CheB | arr19 | MMP0925 CheW | | MMP0927 | HKVI | ahk42 | MMP0928 CheD | | MMP0933 | RRI-CheY | arr7 | MMP0929 mcp | | MMP1303 | HKIV | ahk32 | | | MMP1304 | RRI-CheY | arr2 | | | | | | | Methanosarcina acetivorans | | | | | MA0014 | HKVI | ahk41 | | | MA0015 | RRI-CheB | arr19 | | | MA0016 | RRI-CheY | arr10 | | | MA0018 | RRI-CheY | arr16 | MA0019 mcp | | | | MA0020 CheW | | Methanosarcina acetivorans cont’d | | | | | MA0551 | HKII + PASPAC | | | | MA0552 | HKIII | ahk9 | | | MA0619 | HKIII | ahk12 | | | MA0620 | HKIII | ahk14 | | | MA0758 | HKIII | | | | MA0759 | HKIII | ahk30 | | | MA1267 | HYI + PASPAC | ahy2 | | | MA1268 | RRI-CheY | arr9 | | | MA1269 | RRI-CheY | | | | MA1270 | HKII + PASPAC | | | | MA1468 | RRI-CheY | | | | MA1469 | RRI-CheY | arr8 | | | MA1470 | HKIII | ahk8 | | | MA1627 | HKIII | ahk25 | | | MA1628 | HKII + PASPAC | ahk4 | | | MA1645 | HKIII | ahk17 | | | MA1646 | HKII + PASPAC | ahk6 | | | MA2012 | RRI-CheY | | | | MA2013 | HYII + Hpt | | | | MA3066 | HKVI | ahk40 | MA3063 CheR | | MA3068 | RRI-CheY | arr7 | MA3064 CheD | | MA3067 | RRI- CheB | arr18 | MA3065 CheC | | | | MA3070 CheW | | MA3368 | HKIII | ahk24 | | | MA3370 | HKII + PASPAC | | | | MA4376 | RRI-CheY | arr12 | | | MA4377 | HYIII CHSE4HP | ahy7 | | | | | | | Methanosracina barkeri | | | | | MbarA_0984 | HKVI | ahk41 | MbarA_0983 CheR | | MbarA_0985 | RRIV-CheB | arr19 | | | MbarA_0986 | RRI-CheY | arr10 | | | MbarA_0988 | RRI-CheY | | MbarA_0989 mcp | | Opp orientation to above | | | MbarA_0990 CheW | | MbarA_1051 | RRI-CheY | arr12 | | | MbarA_1052 | HYIII | ahy7 | | | MbarA_3036 | HKII | | | | MbarA_3037 | HKII | | | | MbarA_3247 | HYIPASPAC | | | | MbarA_3248 | RRI-CheY | | | | MbarA_3250 | HKII | | | | MbarA_3447 | HKII | | | | MbarA_3448 | | | | | | | | | Methanosracina mazei | | | | | MM0168 | HKII | ahk9 | | | MM0169 | HKIII | | | | MM0328 | HKVI | ahk40 | MM3025 CheR | | MM0329 | RRI- CheB | arr18 | MM0326 CheD | | MM0330 | RRI-CheY | arr7 | MM0327 CheC | | | | MM0332 CheW | | | | MM0333 mcp | | MM1325 | HKVI | ahk41 | MM1323 CheC | | MM1326 | RRI-CheY | arr19 | MM1324 | | MM1327 | | arr10 | CheB | | MM1328 opp orientation to above | RRI-CheY | arr16 | MM1329 mcp | | | | MM1330 CheW | | Methanosracina mazei cont’d. | | | | | MM2275 | HKIII | ahk28 | | | MM2276 | HKIII | | | | MM2277 | HKIII | | | | MM2515 | HKIII | ahk8 | | | MM2516 | RRI-CheY | arr8 | | | MM2880 | RRI-CheY | arr3 | | | MM2881 | HYIII | ahy6 | | | MM2953 | RRI-CheY | arr4 | | | MM2954 | RRI-CheY | arr5 | | | MM2955 | HKVIPASPACCach | | | | MM3205 | HYIII | | | | MM3206 | RRI-CheY | | | | | | | | Pyrococcus abyssi | | | | | PAB1330 | RRI-CheY | arr7 | PAB1329 CheR | | PAB1331 | RRVI-CheB | arr19 | PAB1333 CheC | | PAB1332 | HKVI | ahk42 | PAB1334 CheC | | | | PAB1335CheW | | | | PAB1336 mcp | | | | | | Pyrococcus horikoshi | | | | | PH0482 | RRI-CheY | arr7 | PH0481 CheB | | PH0483 | RRIV-CheB | arr19 | | | PH0484 | HKVI | ahk42 | |
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