Phylogenomics of the archaeal flagellum: rare horizontal gene transfer in a unique motility structure
© Desmond et al; licensee BioMed Central Ltd. 2007
Received: 28 February 2007
Accepted: 02 July 2007
Published: 02 July 2007
As bacteria, motile archaeal species swim by means of rotating flagellum structures driven by a proton gradient force. Interestingly, experimental data have shown that the archaeal flagellum is non-homologous to the bacterial flagellum either in terms of overall structure, components and assembly. The growing number of complete archaeal genomes now permits to investigate the evolution of this unique motility system.
We report here an exhaustive phylogenomic analysis of the components of the archaeal flagellum. In all complete archaeal genomes, the genes coding for flagellum components are co-localized in one or two well-conserved genomic clusters showing two different types of organizations. Despite their small size, these genes harbor a good phylogenetic signal that allows reconstruction of their evolutionary histories. These support a history of mainly vertical inheritance for the components of this unique motility system, and an interesting possible ancient horizontal gene transfer event (HGT) of a whole flagellum-coding gene cluster between Euryarchaeota and Crenarchaeota.
Our study is one of the few exhaustive phylogenomics analyses of a non-informational cell machinery from the third domain of life. We propose an evolutionary scenario for the evolution of the components of the archaeal flagellum. Moreover, we show that the components of the archaeal flagellar system have not been frequently transferred among archaeal species, indicating that gene fixation following HGT can also be rare for genes encoding components of large macromolecular complexes with a structural role.
Motile archaeal species swim by means of rotating flagellum structures driven by a proton gradient force [1, 2], as in bacteria . Interestingly, although they are both responsible for swimming, archaeal and bacterial flagella are not homologous, either in terms of overall structure, components and assembly (for a recent review see [4, 5]). The bacterial flagellum is a complex rotary structure made up of as much as 20 proteins and composed of three major parts -the basal body, the hook, and the filament. Rotation is provided by an ATPase exploiting a proton gradient force, and can be switched by specific proteins in response to attractants or repellents in the environment through the chemotaxis system. The filament is a hollow structure about 20 nm in diameter and is composed of a single type of protein called flagellin. Bacterial flagellins are assembled by a complex type III secretion system located in the basal body and are added to the distal tip of the flagellum after passing through the hollow cavity .
Much less is known about the archaeal flagellum. It has been extensively studied in terms of components, assembly, and mutation experiments, in Halobacteria and Methanococcales (for recent reviews [4–6]). The archaeal flagellum is a structure thinner than its bacterial counterpart, where at least a filament and a hook are evident [7–9]. The archaeal flagellum has been shown to have a unique symmetry in Halobacterium salinarium. In fact, it has 3.3 subunits/turn of a 1.9 nm pitch left-handed helix compared to 5.5 subunits/turn of a 2.6 nm pitch right-handed helix for plain bacterial flagellum filaments [10, 11]. The archaeal filament can be made up of different types of homologous flagellin proteins (called FlaA or FlaB). The filament is ~10 nm in diameter and is not hollow, resembling more to bacterial type IV pili in this respect . A few other characteristics of archaeal flagella make them more alike bacterial pili than flagella: as bacterial pilins, archaeal flagellins (i) are made as preproteins with short signal peptides that are processed by a recently identified archaeal-specific signal peptidase (called FlaK) [12–14] that shows weak sequence similarity with the bacterial pili leader peptidase PilD, (ii) are likely added at the base of the filament as in bacterial pili, and (iii) undergo glycosylation as post-translational modification  (see  for a recent review). Moreover, one component of archaeal flagella (FlaI) is homologous to bacterial PilT, an ATPase involved in bacterial pilin export (a type II/IV secretion system) and pilus retraction during twitching motility . However, none of the remaining archaeal flagellum components are homologous to those of bacterial pili . Moreover, bacterial pili are not rotating structures, and no specific anchoring structures have ever been observed, indicating substantial differences between these two cellular structures.
A number of putative flagellum accessory genes lie close to flagellin genes in archaeal genomes (called flaC, flaD/flaE, flaF, flaG, flaH, flaI, and flaJ) . Their putative role in flagellum structure and assembly was tentatively deduced based on their sequences, cellular location, and mutation experiments [4–6].
FlaC, FlaD, FlaH and FlaI are associated with the membrane fraction in Methanococcus voltae and may thus be peripheral components of the archaeal flagellum [5, 6]. FlaH, FlaI and FlaJ may be important for the assembly of archaeal flagella and possibly form a secretion complex [5, 6]. FlaH harbors a domain similar to that found in bacterial RecA-like ATPases, and FlaH mutants are nonmotile and nonflagellated . FlaJ contains many transmembrane domains, while FlaI probably encodes an ATPase that may be important for flagellins export, similarly to the role of its bacterial homologue, the pilin export ATPase PilT, and/or for providing the force for rotation. No experimental data are presently available for FlaG and FlaF, although FlaG may be a component of the anchoring system between the hook and the filament . It may be possible that some of the multiple flagellin proteins have different roles in flagellum substructures other than the filament . Finally, additional components of the archaeal flagellum may be encoded by genes that have not yet been identified.
The uniqueness of the archaeal flagellum in terms of components, structure, and assembly indicates that archaeal and bacterial flagella have distinct origins (i.e. they are analogous systems). Interestingly, homologues of most bacterial chemotaxis genes are found in archaeal genomes [5, 18], suggesting that archaeal and bacterial chemotaxis systems are evolutionary related. However, their interaction with the flagellum system in Archaea remains largely unknown (for a recent review see ). In this work, we sought to contribute to the research on archaeal flagella and archaeal motility in general performing an accurate phylogenomic study (sensu Eisen ) of the archaeal motility apparatus in terms of taxonomic distribution of the genes coding for its components, their genomic context, and their phylogeny. This allowed us to sketch a fairly detailed image on the origin and evolution of this macromolecular structure.
Taxonomic distribution and genomic context
A careful observation of gene order within each cluster revealed two types of organizations, that we will hereafter call fla 1 and fla 2 (Figure 2). fla 1 clusters are characterized by the presence of flaC, plus one or few copies of flaD (also annotated as flaE), or by a fusion of flaC and flaD (Figure 2A), whereas fla 2 clusters lack these genes (Figure 2B). Nevertheless, psi-Blast searches revealed that the genes (hyp1 and hyp2, Figure 2B) lying between flaB and flaG in fla 2 clusters from Methanomicrobia (Methanosarcinales and the Methanomicrobiale Methanospirillum hungatei) and Archaeoglobales may be a very distant homologue of flaD, as already suggested . A second characteristic differentiates fla 1 and fla 2 clusters: they show an inverted order of flaG and flaF. While the gene order in fla 1 clusters is flaB-flaC-flaD- flaF-flaG -flaH-flaI-flaJ, fla 2 clusters (lacking flaC/D) display the order flaB- flaG-flaF -flaH-flaI-flaJ (Figure 2). Interestingly, all the archaeal genomes contain only a single type of fla clusters (i.e. fla 1 or fla 2), except M. burtonii that is the only species that harbors both type I and II fla clusters. fla 1 clusters are present only in Euryarchaeota: Thermococcales (Pyrococcus abyssi, Pyrococcus furiosus, Pyrococcus horikoshii and Thermococcus kodakarensis), Methanococcales (Methanocaldococcus jannashii and Methanococcus maripaludis), Thermoplasmatales (Thermoplasma acidophilum and Thermoplasma volcanium), Halobacteriales (Haloarcula marismortuii, Halobacterium sp. and Natromonas pharaonis), and Methanomicrobia(Methanococcoides burtonii) (Figure 2A); whereas fla 2 clusters are present in Crenarchaeota: Desulfurococcales (Aeropyrum pernix) and Sulfolobales (Sulfolobus solfataricus Sulfolobus tokodaii Sulfolobus acidocaldarius) and in some Euryarchaeota: Methanomicrobia (Methanospirillum hungatei, Methanococcoides burtonii, Methanosarcina acetivorans, Methanosarcina mazei and Methanosarcina barkeri) and the Archaeoglobale Archaeoglobus fulgidus (Figure 2B). In Halobacteriales and Sulfolobales the clusters also include non-flagellum genes (Figure 2A). In particular, a gene coding for a homologue of a bacterial chemotaxis component (MCP domain signal transducer) is present in Halobacterium sp., and three genes coding for components of the chemotaxis system are present in H. marismortui (CheY, CheA, and CheD) and in N. pharaonis (CheY, CheC, and CheD). In this archaeon, the operon is disrupted, the second half lying at ~50 ORFs downstream (Figure 2A). Interestingly,M. mazei and M. acetivorans each harbor two copies of the fla 2 cluster (hereafter called fla 2A and fla 2B), that differ in the number of flagellin gene copies (two in fla 2A and one in fla 2B), and in the presence of two different hypothetical genes (possibly very distant homologues of flaD, see above) lying in between the genes coding for FlaB and FlaG (Figure 2B). According to these characteristics, the A. fulgidus, the M. hungatei and one of the M. burtonii gene clusters resemble more to the fla 2A cluster, while that from M. barkeri resembles more to the fla 2B cluster (Figure 2B). Multiple copies of flagellin genes (flaB/flaA) are found in most archaeal genomes, especially in Thermococcales, whereas Thermoplasmatales and Sulfolobales harbor single gene copies (Figure 2), confirming earlier studies on the composition of the flagella from T. volcanium and S. shibatae . In M. hungatei, the flagellin genes lie in another region of the chromosome (two are clustered together and an additional small one is isolated (Figure 2B)), suggesting a disruption of the original cluster. This is also the case of the fla 1 cluster of M. burtonii, which presents no nearby flagellin genes (a single isolated flaB gene was possibly part of this cluster before disruption, Figure 2A and see below). In S. solfataricus a transposase disrupts the gene coding for FlaG (Figure 2B). However, both the N- and C-ter sequences of FlaG are still very similar to FlaG homologues found in S. solfataricus close relatives (e.g. S. acidocaldarius and S. tokodaii), suggesting that the disruption of flaG is recent. Indeed, the sequenced genome of S. solfataricus presents indeed a high number of insertion elements that may have recently invaded this strain . Interestingly, cells of this strain appear non-flagellated under the electron microscope (P. Redder, personal communication) even if the disruption of the flaG gene does not affect the transcription of the downstream operon genes . This suggests that FlaG (possibly involved in the flagellum anchoring system ) is an essential flagellum component.
Finally, additional copies of flagellum components lie in a few instances outside of the clusters (examples are additional flaB genes in M. burtonii, the two Thermoplasmatales, H. marismortui and N. pharaonis; an additional flaG in Halobacterium sp.; an additional flaD in H. marismortui, N. pharaonis, and M. burtonii; an additional flaF in M. maripaludis, and an additional flaK in Methanococcales) (Figure 2).
Phylogenetic analyses were performed on six amino acid sequence datasets corresponding to FlaA/B, FlaD/E, FlaG, FlaH, FlaI, and FlaJ. Phylogenetic analysis of FlaC, FlaF and FlaK could not be performed due to a too restricted phylogenetic distribution of FlaC, and the poor sequence conservation of FlaF and FlaK.
FlaG, FlaH, FlaI, FlaJ
Among all archaeal flagellum components, FlaH, FlaI and FlaJ are the most conserved at the sequence level and always lie close to each other in all the analyzed genomes (Figure 2) strengthening their likely fundamental role in flagellum assembly and function (see above). FlaI has a number of bacterial homologues belonging to type IV and type II secretion systems, including the typeIV pili component PilT . Moreover, FlaI has additional archaeal homologues that are also probably part of yet to describe secretion machineries [27, 28]. In a phylogeny including all these homologues FlaI sequences form a monophyletic group and are most closely related to their archaeal counterparts (not shown). FlaH shares a RecA-like ATPase domain with distant archaeal and bacterial homologues that are not involved in motility structures. Psi-blast searches revealed (i) that FlaJ harbours a few distant archaeal homologues annotated as involved in type II secretion and (ii) weak similarities with the bacterial pilus assembly protein TadC and TadB.
FlaJ shares the domain GSPII F with TadC and TadB. However, this may not be significant, given that the domain was defined on the basis of an alignment that included both archaeal and bacterial sequences. The similarity between the FlaJ sequences and TadB and TadC sequences is very weak (16% and 35% of identity and similarity with TadB sequences, respectively and 14% and 32% of identity and similarity with TadC sequences, respectively) and is mainly the result of the sharing of small hydrophobic amino acids. To our point of view this sequence similarity is too weak to definitively conclude that these sequences are homologues although this has been claimed .
Given the use of only 72 unambiguously aligned positions for analysis, the FlaB tree presents a number of poorly resolved nodes (Figure 4B). Nevertheless, the monophyly of a number of groups is recovered and supported by BV > 850‰, except for Thermococcales, Methanococcales and Methanomicrobia. As for FlaG, FlaI, FlaJ, and FlaH, the FlaB tree is again strongly consistent with gene cluster organization (Figure 4B). In particular, the FlaB from the fla 2 clusters of M. hungatei, the four Methanosarcinales and A. fulgidus appear close to Crenarchaeota, while the isolated FlaB from M. burtonii appear close to Halobacteria, and thus likely functions with the flagellum components of fla 1 cluster (Figure 4B). Interestingly, the multiple copies of flagellins group in a group-specific manner (Figure 4B), suggesting that flagellin gene family expansion occurred mainly by gene duplication and multiple times independently in different species, and not by HGT.
Discussion and conclusion
Both scenarios imply that the archaeal flagellum would have appeared prior to the last archaeal ancestor
Apart these two likely cases of HGT of the entire fla 2 gene cluster, we found no clear evidence for recent transfers of the genes coding for flagellum components among archaeal species. Indeed, the poor resolution of inter-phyla relationships in some trees is more likely due to lack of phylogenetic signal rather than horizontal gene transfer. One explanation for the rarity of HGT is that it is possible the result of the high level of integration of flagellum components within the macromolecular structure. Importantly, this contradicts the generally assumed notion that HGT of "informational" genes (i.e. those coding for proteins involved in the expression and the transmission of genetic information) are less frequent than those involving the remaining ones ("operational") genes. Nevertheless, the acquisition of a whole flagellum component coding gene cluster from distant donors seems possible. Interestingly, even if two clusters coexist within a genome (i.e. in M. burtonii) neither gene recombination is observed between homologous genes belonging to the two clusters, nor losses, suggesting that the components of a cluster may interact preferentially due to coevolution, although they form similar cellular structures. The presence in M. burtonii of two types of fla clusters (possibly one native and one acquired by HGT from crenarchaeota) represents an interesting experimental model to study. It would be in fact particular interesting to know the difference between the components encoded by the two fla clusters in terms of expression and assembly, and how two different flagellum systems coexist in this archaeon.
Finally, it has been suggested that archaea are modified Actinobacteria and that archaeal flagella are derived from bacterial flagella following an adaptation to acidic environments by the recruitment of an already acid-stable glycoprotein from the pilus machinery that would have replaced the original flagellin while leaving intact the basal rotary motor . We find this hypothesis unlikely for the fact that archaeal flagella do not resemble to bacterial flagella in major structure, assembly, and components, and not only concerning flagellin. Indeed, no even distant homologues to any component, including the basal rotary motor, of bacterial flagella can be recovered in archaeal genomes, including the related type III secretion system components . Moreover, flagella of acidophilic bacteria (such as Thiobacillus) show a typical bacterial structure (e.g. a diameter of approximately 20 nm), so they adapted to acidic conditions without radically modifying their motility structures and components . Indeed, the uncomplete genome of the extreme acidophilic bacterium (optimal pH<3) Acidobacterium capsulatum contains a clear homologue of bacterial flagellin, indicating that adaptation to acidic environments was possible without its replacement.
The lack of congruence between the description of archaeal species as motile or non-motile and the taxonomic distribution of homologues of flagellum component coding genes is particularly striking and underlines the need to explore more in depth the motility systems in Archaea. The presence of two gene clusters in non motile Methanosarcinales is particularly puzzling. Either these species can be flagellated under particular conditions that have not yet been tested, or the flagellum component homologues are involved in other functions than motility (for example, they could be required for cell-cell adhesion to form cell aggregates, a peculiarity of this archaeal family). It will be extremely interesting to study the expression and localization of the flagellum components in Methanosarcinales, in the light of the fact that the flagellum genes of Methanosarcinales may have been recruited from the distantly related Crenarchaeota, since this event may have been an important step in the evolution of this archaeal lineage. Moreover, virtually nothing is known about other types of motility than swimming in archaea , while in bacteria these are starting being investigated . The fact that no homologues of flagellum components are encoded in the genomes of at least two archaeal species that are described as motile (M. kandleri and P. aerophilum) is also puzzling. Although it is possible that the strains used for genome sequencing have lost the flagellum operon following lab cultivation (see for example , it would surely be interesting to test motility in these archaeal species. Alternatively, this observation could also suggest that other types of motility may occur in archaea and are made possible by still unknown molecular structures. It would also be very useful to investigate the relationship between the flagellum and the secretion systems in Archaea. Indeed, archaeal genomes harbor only a few homologues of bacterial TypeII/IV secretion systems , and it is not known whether they form pili, despite rare observations [33–35] and evidence for conjugation [36–38].
To sum up, two radically different options for motility were adopted at the divergence of the two prokaryotic domains, and much still remain to be uncovered on archaeal motility systems.
Data set construction
The list of archaeal flagellum components was retrieved from the Kyoto Encyclopedia of Genes and Genomes . Homologous sequences of each archaeal flagellum component were retrieved from the nr database at the National Center for Biotechnology Information  using the BlastP program with different seeds  and the ALIBABA program (P. Lopez personal communication). For each dataset, additional searches using psi-Blast were performed to search for divergent homologues (especially from bacteria) . tBlastN searches on the unfinished genomes of the Halobacteriale Haloferax volcanii were performed at TIGR . Multiple alignments were done with ClustalW  and MUSCLE . For each dataset, the quality of the alignments obtained with CLUSTALW and MUSCLE, was evaluated with T-COFFEE (CLUSTALW and MUSCLE provided alignments of comparable quality, not shown) . All the alignments were edited and manually improved using the ED program from the MUST package . Regions where the homology between sites was doubtful were manually removed from the datasets for phylogenetic analyses.
Maximum Likelihood (ML) phylogenetic trees were computed with Phyml [47, 48] and the JJT model of amino acid substitution (Jones, Taylor and Thornton . A gamma correction with 4 discrete classes of sites was used to take into account the heterogeneity of evolutionary rates across sites. The alpha parameter and the proportion of invariable sites were estimated for each dataset. The robustness of each branch was estimated by non-parametric bootstrap analysis (1000 replicates) using PHYML. In addition, bayesian analyses were performed using MrBayes  with a mixed model of amino acid substitution. As for ML tree reconstruction, a gamma correction with 4 discrete classes of sites was used and the alpha parameter and the proportion of invariable sites were estimated. MrBayes was run with four chains for 1 million generations and trees were sampled every 100 generations. To construct the consensus tree, the first 1500 trees were discarded as "burnin".
Genomic context analysis
The genomic localization of each archaeal flagellum component was manually investigated in all archaeal complete genomes available at the NCBI.
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