Accounting for Horizontal Gene Transfers Explains Conflicting Hypotheses Regarding the Position of Aquificales in the Phylogeny of Bacteria

Overview

Journal BMC Evol Biol

Publisher Biomed Central

Specialty Biology

Date 2008 Oct 7

PMID 18834516

Citations 41

Authors

Bastien Boussau

Laurent Gueguen

Manolo Gouy

Affiliations

Soon will be listed here.

Abstract

Background: Despite a large agreement between ribosomal RNA and concatenated protein phylogenies, the phylogenetic tree of the bacterial domain remains uncertain in its deepest nodes. For instance, the position of the hyperthermophilic Aquificales is debated, as their commonly observed position close to Thermotogales may proceed from horizontal gene transfers, long branch attraction or compositional biases, and may not represent vertical descent. Indeed, another view, based on the analysis of rare genomic changes, places Aquificales close to epsilon-Proteobacteria.

Results: To get a whole genome view of Aquifex relationships, all trees containing sequences from Aquifex in the HOGENOM database were surveyed. This study revealed that Aquifex is most often found as a neighbour to Thermotogales. Moreover, informational genes, which appeared to be less often transferred to the Aquifex lineage than non-informational genes, most often placed Aquificales close to Thermotogales. To ensure these results did not come from long branch attraction or compositional artefacts, a subset of carefully chosen proteins from a wide range of bacterial species was selected for further scrutiny. Among these genes, two phylogenetic hypotheses were found to be significantly more likely than the others: the most likely hypothesis placed Aquificales as a neighbour to Thermotogales, and the second one with epsilon-Proteobacteria. We characterized the genes that supported each of these two hypotheses, and found that differences in rates of evolution or in amino-acid compositions could not explain the presence of two incongruent phylogenetic signals in the alignment. Instead, evidence for a large Horizontal Gene Transfer between Aquificales and epsilon-Proteobacteria was found.

Conclusion: Methods based on concatenated informational proteins and methods based on character cladistics led to different conclusions regarding the position of Aquificales because this lineage has undergone many horizontal gene transfers. However, if a tree of vertical descent can be reconstructed for Bacteria, our results suggest Aquificales should be placed close to Thermotogales.

Citing Articles

Discovery of a Biotin Synthase That Utilizes an Auxiliary 4Fe-5S Cluster for Sulfur Insertion.

Lachowicz J, Lennox-Hvenekilde D, Myling-Petersen N, Salomonsen B, Verkleij G, Acevedo-Rocha C J Am Chem Soc. 2024; 146(3):1860-1873.

PMID: 38215281 PMC: 10813225. DOI: 10.1021/jacs.3c05481.

Identification of a deep-branching thermophilic clade sheds light on early bacterial evolution.

Leng H, Wang Y, Zhao W, Sievert S, Xiao X Nat Commun. 2023; 14(1):4354.

PMID: 37468486 PMC: 10356935. DOI: 10.1038/s41467-023-39960-x.

Was the Last Bacterial Common Ancestor a Monoderm after All?.

Leonard R, Sauvage E, Lupo V, Perrin A, Sirjacobs D, Charlier P Genes (Basel). 2022; 13(2).

PMID: 35205421 PMC: 8871954. DOI: 10.3390/genes13020376.

Dissecting the dominant hot spring microbial populations based on community-wide sampling at single-cell genomic resolution.

Bowers R, Nayfach S, Schulz F, Jungbluth S, Ruhl I, Sheremet A ISME J. 2021; 16(5):1337-1347.

PMID: 34969995 PMC: 9039060. DOI: 10.1038/s41396-021-01178-4.

Phylogenetic Signal, Congruence, and Uncertainty across Bacteria and Archaea.

Martinez-Gutierrez C, Aylward F Mol Biol Evol. 2021; 38(12):5514-5527.

PMID: 34436605 PMC: 8662615. DOI: 10.1093/molbev/msab254.

References

Castresana J . Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000; 17(4):540-52. DOI: 10.1093/oxfordjournals.molbev.a026334. View

Shimodaira H . An approximately unbiased test of phylogenetic tree selection. Syst Biol. 2002; 51(3):492-508. DOI: 10.1080/10635150290069913. View

Wolf Y, Aravind L, Grishin N, Koonin E . Evolution of aminoacyl-tRNA synthetases--analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res. 1999; 9(8):689-710. View

Daubin V, Gouy M, Perriere G . A phylogenomic approach to bacterial phylogeny: evidence of a core of genes sharing a common history. Genome Res. 2002; 12(7):1080-90. PMC: 186629. DOI: 10.1101/gr.187002. View

Brinkmann H, van der Giezen M, Zhou Y, Poncelin de Raucourt G, Philippe H . An empirical assessment of long-branch attraction artefacts in deep eukaryotic phylogenomics. Syst Biol. 2005; 54(5):743-57. DOI: 10.1080/10635150500234609. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Galtier N, Lobry J . Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J Mol Evol. 1997; 44(6):632-6. DOI: 10.1007/pl00006186. View

Weisburg W, Giovannoni S, Woese C . The Deinococcus-Thermus phylum and the effect of rRNA composition on phylogenetic tree construction. Syst Appl Microbiol. 1989; 11:128-34. DOI: 10.1016/s0723-2020(89)80051-7. View

Iyer L, Koonin E, Aravind L . Evolution of bacterial RNA polymerase: implications for large-scale bacterial phylogeny, domain accretion, and horizontal gene transfer. Gene. 2004; 335:73-88. DOI: 10.1016/j.gene.2004.03.017. View

10.

Dutheil J, Gaillard S, Bazin E, Glemin S, Ranwez V, Galtier N . Bio++: a set of C++ libraries for sequence analysis, phylogenetics, molecular evolution and population genetics. BMC Bioinformatics. 2006; 7:188. PMC: 1501049. DOI: 10.1186/1471-2105-7-188. View

11.

Shimodaira H, Hasegawa M . CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics. 2001; 17(12):1246-7. DOI: 10.1093/bioinformatics/17.12.1246. View

12.

Bern M, Goldberg D . Automatic selection of representative proteins for bacterial phylogeny. BMC Evol Biol. 2005; 5:34. PMC: 1175084. DOI: 10.1186/1471-2148-5-34. View

13.

Foster P, Hickey D . Compositional bias may affect both DNA-based and protein-based phylogenetic reconstructions. J Mol Evol. 1999; 48(3):284-90. DOI: 10.1007/pl00006471. View

14.

Kreil D, Ouzounis C . Identification of thermophilic species by the amino acid compositions deduced from their genomes. Nucleic Acids Res. 2001; 29(7):1608-15. PMC: 31282. DOI: 10.1093/nar/29.7.1608. View

15.

Schutz M, Brugna M, Lebrun E, Baymann F, Huber R, Stetter K . Early evolution of cytochrome bc complexes. J Mol Biol. 2000; 300(4):663-75. DOI: 10.1006/jmbi.2000.3915. View

16.

Beiko R, Harlow T, Ragan M . Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A. 2005; 102(40):14332-7. PMC: 1242295. DOI: 10.1073/pnas.0504068102. View

17.

Klenk H, Meier T, Durovic P, Schwass V, Lottspeich F, Dennis P . RNA polymerase of Aquifex pyrophilus: implications for the evolution of the bacterial rpoBC operon and extremely thermophilic bacteria. J Mol Evol. 1999; 48(5):528-41. DOI: 10.1007/pl00006496. View

18.

Schopf J . Fossil evidence of Archaean life. Philos Trans R Soc Lond B Biol Sci. 2006; 361(1470):869-85. PMC: 1578735. DOI: 10.1098/rstb.2006.1834. View

19.

Hrdy I, Hirt R, Dolezal P, Bardonova L, Foster P, Tachezy J . Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature. 2004; 432(7017):618-22. DOI: 10.1038/nature03149. View

20.

Jones D, Taylor W, Thornton J . The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992; 8(3):275-82. DOI: 10.1093/bioinformatics/8.3.275. View