An automated approach for the identification of horizontal gene transfers from complete genomes reveals the rhizome of Rickettsiales

BMC Evolutionary Biology

Pierre Pontarotti²  Dider Raoult¹  Olivier Chabrol²  Philippe Gouret²  Julien Paganini²  Laurent Guijarro²  Hemalatha Golaconda Ramulu¹  Phuong Thi Le¹ 

[1] Unit for Research on Emergent and Tropical Infectious Diseases, URMITE UMR CNRS 7278, IRD 198, Inserm 1095, Aix-Marseille University, Marseille, 13005, France;Evolutionary biology and modeling, LATP UMR-CNRS 7353, Aix-Marseille University, Marseille, 13331, France

关键词: Sympatry;    Candidatus Pelagibacter ubique;    Rickettsiales;    Horizontal gene transfer;   

Others  :  1139888
DOI  :  10.1186/1471-2148-12-243

 received in 2012-08-23, accepted in 2012-11-22,  发布年份 2012

【 摘 要 】

Background

Horizontal gene transfer (HGT) is considered to be a major force driving the evolutionary history of prokaryotes. HGT is widespread in prokaryotes, contributing to the genomic repertoire of prokaryotic organisms, and is particularly apparent in Rickettsiales genomes. Gene gains from both distantly and closely related organisms play crucial roles in the evolution of bacterial genomes. In this work, we focus on genes transferred from distantly related species into Rickettsiales species.

Results

We developed an automated approach for the detection of HGT from other organisms (excluding alphaproteobacteria) into Rickettsiales genomes. Our systematic approach consisted of several specialized features including the application of a parsimony method for inferring phyletic patterns followed by blast filter, automated phylogenetic reconstruction and the application of patterns for HGT detection. We identified 42 instances of HGT in 31 complete Rickettsiales genomes, of which 38 were previously unidentified instances of HGT from Anaplasma, Wolbachia, Candidatus Pelagibacter ubique and Rickettsia genomes. Additionally, putative cases with no phylogenetic support were assigned gene ontology terms. Overall, these transfers could be characterized as “rhizome-like”.

Conclusions

Our analysis provides a comprehensive, systematic approach for the automated detection of HGTs from several complete proteome sequences that can be applied to detect instances of HGT within other genomes of interest.

【 授权许可】

   
2012 Le et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 2.

【 参考文献 】

• [1]Doolittle WF: Lateral genomics. Trends in Cell Biol 1999, 9(12):M5—8.
• [2]Koonin EV, Makarova KS, Aravind L: Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 2001, 55:709-742.
• [3]Ochman H, Lawrence JG, Groisman EA: Lateral gene transfer and the nature of bacterial innovation. Nature 2000, 405(6784):299-304.
• [4]Jain R, Rivera MC, Moore JE, Lake JA: Horizontal gene transfer accelerates genome innovation and evolution. Mol biol evol 2003, 20(10):1598-1602.
• [5]Merhej V, Royer-Carenzi M, Pontarotti P, Raoult D: Massive comparative genomic analysis reveals convergent evolution of specialized bacteria. Biol Direct 2009, 4:13. BioMed Central Full Text
• [6]Boussau B, Karlberg EO, Frank AC, Legault BA, Andersson SGE: Computational inference of scenarios for alpha-proteobacterial genome evolution. Proc National Acad Sci USA 2004, 101(26):9722-9727.
• [7]PHILIP CB: Tsutsugamushi disease in World War II. J Parasitology 1948, 34(3):169-191.
• [8]Seong SY, Choi MS, Kim IS: Orientia tsutsugamushi infection: overview and immune responses. Microbes and Infection / Institut Pasteur 2001, 3:11-21.
• [9]Tamura A, Ohashi N, Urakami H, Miyamura S: Classification of Rickettsia tsutsugamushi in a new genus, Orientia gen. nov., as Orientia tsutsugamushi comb. nov. Int J Syst Bacteriol 1995, 45(3):589-591.
• [10]Raoult D, Roux V: Rickettsioses as paradigms of new or emerging infectious diseases. Clin Microbio Rev 1997, 10(4):694-719.
• [11]Merhej V, Raoult D: Rickettsial evolution in the light of comparative genomics. Biol Rev Cambridge Philos Soc 2011, 86(2):379-405.
• [12]Anderson CL, Karr TL: Wolbachia: evolutionary novelty in a rickettsial bacteria. BMC Evol Biol 2001, 1:10. BioMed Central Full Text
• [13]Chen SM, Dumler JS, Bakken JS, Walker DH: Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 1994, 32(3):589-595.
• [14]Anderson BE, Dawson JE, Jones DC, Wilson KH: Ehrlichia chaffeensis, a new species associated with human ehrlichiosis. J Clin Microbiol 1991, 29(12):2838-2842.
• [15]Dawson JE, Anderson BE, Fishbein DB, Sanchez JL, Goldsmith CS, Wilson KH, Duntley CW: Isolation and characterization of an Ehrlichia sp. from a patient diagnosed with human ehrlichiosis. J Clin Microbiol 1991, 29(12):2741-2745.
• [16]Rikihisa Y: The tribe Ehrlichieae and ehrlichial diseases. Clin microbiol rev 1991, 4(3):286-308.
• [17]Nikoh N, Tanaka K, Shibata F, Kondo N, Hizume M, Shimada M, Fukatsu T: Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 2008, 18(2):272-280.
• [18]Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, Bibbs L, Eads J, Richardson TH, Noordewier M, Rappé MS, Short JM, Carrington JC, Mathur EJ: Genome streamlining in a cosmopolitan oceanic bacterium. Sci (New York, N.Y.) 2005, 309(5738):1242-1245.
• [19]Williams KP, Sobral BW, Dickerman AW: A robust species tree for the alphaproteobacteria. J bacteriol 2007, 189(13):4578-4586.
• [20]Georgiades K, Madoui MA, Le P, Robert C, Raoult D: Phylogenomic analysis of Odyssella thessalonicensis fortifies the common origin of Rickettsiales, Pelagibacter ubique and Reclimonas americana mitochondrion. PloS one 2011, 6(9):e24857.
• [21]Thrash JC, Boyd A, Huggett MJ, Grote J, Carini P, Yoder RJ, Robbertse B, Spatafora JW, Rappé MS, Giovannoni SJ: Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Sci rep 2011, 1:13.
• [22]Viklund J, Ettema TJG, Andersson SGE: Independent Genome Reduction and Phylogenetic Reclassification of the Oceanic SAR11 Clade. Mol Biol Evol 2011, 29(2):599-615.
• [23]Brindefalk B, Ettema TJG, Viklund J, Thollesson M, Andersson SGE: A Phylometagenomic Exploration of Oceanic Alphaproteobacteria Reveals Mitochondrial Relatives Unrelated to the SAR11 Clade. PloS One 2011, 6(9):e24457.
• [24]Rodráguez-Ezpeleta N, Embley TM: The SAR11 Group of Alpha-Proteobacteria Is Not Related to the Origin of Mitochondria. PloS One 2012, 7:e30520.
• [25]Kloesges T, Popa O, Martin W, Dagan T: Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths. Mol biol evol 2011, 28(2):1057-1074.
• [26]Merhej V, Notredame C, Royer-Carenzi M, Pontarotti P, Raoult D: The rhizome of life: the sympatric Rickettsia felis paradigm demonstrates the random transfer of DNA sequences. Mol Biol Evol 2011, 28(11):3213-3223.
• [27]Georgiades K, Merhej V, El Karkouri K, Raoult D, Pontarotti P: Gene gain and loss events in Rickettsia and Orientia species. Biol Direct 2011, 6:6. BioMed Central Full Text
• [28]Ogata H, La Scola B, Audic S, Renesto P, Blanc G, Robert C, Fournier PE, Claverie JM, Raoult D: Genome sequence of Rickettsia bellii illuminates the role of amoebae in gene exchanges between intracellular pathogens. PLoS Genet 2006, 2(5):e76.
• [29]Blanc G, Ogata H, Robert C, Audic S, Claverie JM, Raoult D: Lateral gene transfer between obligate intracellular bacteria: evidence from the Rickettsia massiliae genome. Genome Res 2007, 17(11):1657-1664.
• [30]Daubin V, Lerat E, Perrière G: The source of laterally transferred genes in bacterial genomes. Genome Biol 2003, 4(9):R57. BioMed Central Full Text
• [31]Lawrence JG, Ochman H: Molecular archaeology of the Escherichia coli genome. Proc National Acad Sci USA 1998, 95(16):9413-9417.
• [32]Hooper SD, Berg OG: Detection of genes with atypical nucleotide sequence in microbial genomes. J mol evol 2002, 54(3):365-375.
• [33]Deschavanne P, Giron A, Vilain J, Dufraigne C, Fertil B: Genomic Signature is Preserved in Short DNA Fragments. IEEE Int Symp Bio-Informatics and Biomed Eng 2000, 33(1):e6.
• [34]Dufraigne C, Fertil B, Lespinats S, Giron A, Deschavanne P: Detection and characterization of horizontal transfers in prokaryotes using genomic signature. Nucleic acids res 2005, 33:e6.
• [35]Shimodaira H: An approximately unbiased test of phylogenetic tree selection. Syst biol 2002, 51(3):492-508.
• [36]Zhaxybayeva O, Hamel L, Raymond J, Gogarten JP: Visualization of the phylogenetic content of five genomes using dekapentagonal maps. Genome biol 2004, 5(3):R20. BioMed Central Full Text
• [37]Zhaxybayeva O, Gogarten JP, Charlebois RL, Doolittle WF, Papke RT: Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome res 2006, 16(9):1099-1108.
• [38]Snel B, Bork P, Huynen MA: Genome phylogeny based on gene content. Nat Genet 1999, 21:108-110.
• [39]Snel B, Bork P, Huynen MA: Genomes in flux: the evolution of archaeal and proteobacterial gene content. Genome Res 2002, 12:17-25.
• [40]David LA, Alm EJ: Rapid evolutionary innovation during an Archaean genetic expansion. Nature 2011, 469(7328):93-96.
• [41]Tatusov RL, Galperin MY, Natale DA, Koonin EV: The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 2000, 28:33-36.
• [42]Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Kiryutin B, Galperin MY, Fedorova ND, Koonin EV: The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 2001, 29:22-28.
• [43]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature genet 2000, 25:25-29.
• [44]Klasson L, Kambris Z, Cook PE, Walker T, Sinkins SP: Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 2009, 10:33. BioMed Central Full Text
• [45]Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC, McGraw EA, Martin W, Esser C, Ahmadinejad N, Wiegand C, Madupu R, Beanan MJ, Brinkac LM, Daugherty SC, Durkin AS, Kolonay JF, Nelson WC, Mohamoud Y, Lee P, Berry K, Young MB, Utterback T, Weidman J, Nierman WC, Paulsen IT, Nelson KE, Tettelin H, O’Neill SL, Eisen JA: Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2004, 2(3):E69.
• [46]Lamrabet O, Merhej V, Pontarotti P, Raoult D, Drancourt M: The genealogic tree of mycobacteria reveals a long-standing sympatric life into free-living protozoa. PloS One 2012, 7(4):e34754.
• [47]Boyer M, Yutin N, Pagnier I, Barrassi L, Fournous G, Espinosa L, Robert C, Azza S, Sun S, Rossmann MG, Suzan-Monti M, La Scola B, Koonin EV, Raoult D: Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc National Acad Sci USA 2009, 106(51):21848-21853.
• [48]Moliner C, Fournier PE, Raoult D: Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol Rev 2010, 34(3):281-94.
• [49]Thomas V, Greub G: Amoeba/amoebal symbiont genetic transfers: lessons from giant virus neighbours. Intervirology 2010, 53(5):254-67.
• [50]Chrisman CJ, Alvarez M, Casadevall A: Phagocytosis of Cryptococcus neoformans by, and nonlytic exocytosis from, Acanthamoeba castellanii. App environ microbiol 2010, 76(18):6056-6062.
• [51]Raoult D, Boyer M: Amoebae as genitors and reservoirs of giant viruses. Intervirology 2010, 53(5):321-9.
• [52]La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D: A giant virus in amoebae. Sci (New York, N.Y.) 2033, 299(5615):2003.
• [53]Scoles GA: Phylogenetic analysis of the Francisella-like endosymbionts of Dermacentor ticks. J Med Entomology 2004, 41(3):277-286.
• [54]Arias MC, Danchin EGJ, Coutinho P, Henrissat B, Ball S: Eukaryote to gut bacteria transfer of a glycoside hydrolase gene essential for starch breakdown in plants. Mobile genet elem 2012, 2(2):81-87.
• [55]Gladyshev EA, Meselson M, Arkhipova IR: Massive horizontal gene transfer in bdelloid rotifers. Sci (New York, N.Y.) 2008, 320(5880):1210-1213.
• [56]Masui S, Kamoda S, Sasaki T, Ishikawa H: Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. J Mol Evol 2000, 51(5):491-497.
• [57]Masui S, Kuroiwa H, Sasaki T, Inui M, Kuroiwa T, Ishikawa H: Bacteriophage WO and virus-like particles in Wolbachia, an endosymbiont of arthropods. Biochem Biophys Res Commun 2001, 283(5):1099-1104.
• [58]Frost LS, Leplae R, Summers AO, Toussaint A: Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 2005, 3(9):722-32.
• [59]Zhao JS, Deng Y, Manno D, Hawari J: Shewanella spp. genomic evolution for a cold marine lifestyle and in-situ explosive biodegradation. PloS one 2010, 5(2):e9109.
• [60]Reen FJ, Almagro-Moreno S, Ussery D, Boyd EF: The genomic code: inferring Vibrionaceae niche specialization. Nat rev Microbiol 2006, 4(9):697-704.
• [61]Caro-Quintero A, Deng J, Auchtung J, Brettar I, Höfle MG, Klappenbach J, Konstantinidis KT: Unprecedented levels of horizontal gene transfer among spatially co-occurring Shewanella bacteria from the Baltic Sea. ISME J 2011, 5:131-140.
• [62]McDaniel LD, Young E, Delaney J, Ruhnau F, Ritchie KB, Paul JH: High frequency of horizontal gene transfer in the oceans. (New York, N.Y.) 2010, 330(6000):50.
• [63]Hazen TH, Pan L, Gu JD, Sobecky PA: The contribution of mobile genetic elements to the evolution and ecology of Vibrios. FEMS Microbiol Ecol 2010, 74(3):485-499.
• [64]Aravind L, Tatusov RL, Wolf YI, Walker DR, Koonin EV: Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends in Genet: TIG 1998, 14(11):442-444.
• [65]Raoult D: The post-Darwinist rhizome of life. Lancet 2010, 375(9709):104-105.
• [66]Cortez D, Forterre P, Gribaldo S: A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol 2009, 10(6):R65. BioMed Central Full Text
• [67]Renesto P, Ogata H, Audic S, Claverie JM, Raoult D: Some lessons from Rickettsia genomics. FEMS, journal=Microbiol Rev. 2005, 29:99-117.
• [68]Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q, Koonin EV, Davis RW: Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Sci (New York, N.Y.) 1998, 282(5389):754-759.
• [69]Zomorodipour A, Andersson SG: FEBS lett. 1999, 452(1-2):11-15.
• [70]Wolf YI, Aravind L, Koonin EV: Rickettsiae and Chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends in Genet: TIG 1999, 15(5):173-175.
• [71]Andersson SG, Zomorodipour A, Andersson JO, Sicheritz-Pontén T, Alsmark UC, Podowski RM, Näslund AK, Eriksson AS, Winkler HH, Kurland CG: The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 1998, 396(6707):133-140.
• [72]Greub G, Raoult D: History of the ADP/ATP-translocase-encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl Environ Microbiol 2003, 69(9):5530-5535.
• [73]Li L, Stoeckert J, Christian J, Roos DS: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13(9):2178-2189.
• [74]Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
• [75]Van Dongen S: Graph clustering by flow simulation. PhD thesis. University of Utrecht, The Netherlands 2000
• [76]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
• [77]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 2011, 28(10):2731-9.
• [78]Gouret P, Thompson JD, Pontarotti P: PhyloPattern: regular expressions to identify complex patterns in phylogenetic trees. BMC Bioinf 2009, 10:298. BioMed Central Full Text
• [79]Warren D, Pereira L, Pereira F: Prolog: the language and its implementation compared with Lisp. In Symposium on Artifical Intelligence and Programming Languages. New York USA: SIGPLAN Notices; 1997:109-15.
• [80]Sankoff D: Minimal mutation trees of sequences. SIAM J App Methamatics, Volume 2835-42. Available at http://ebookbrowse.com/1975-sankoff-pdf-d293771529 webcite
• [81]Chandrasekaran C, Betran E: Origins of new genes and pseudogenes. Nature Education 2008. Available at, http://www.nature.com/scitable/topicpage/origins-of-new-genes-and-pseudogenes-835 webcite
• [82]Gouret P, Vitiello V, Balandraud N, Gilles A, Pontarotti P, Danchin EGJ: FIGENIX: intelligent automation of genomic annotation: expertise integration in a new software platform. BMC Bioinf 2005, 6:198. BioMed Central Full Text
• [83]Paganini J, Gouret P: Reliable Phylogenetic Trees Building: A New Web Interface for FIGENIX. Evolutionary bioinf online 2012, 8:417-421.
• [84]Thompson JD, Higgins DG, Gibson TJ, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic acids res 1994, 22(22):4673-4680.
• [85]Eddy SR: Profile hidden Markov models. Bioinformatics (Oxford, England) 1998, 14(9):755-763.
• [86]Swofford D: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Method). Sunderland, Massachusetts: Sinauer Associates; 2003.
• [87]Schmidt HA, Strimmer K, Vingron M, von Haeseler A: TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics (Oxford, England) 2002, 18(3):502-504.
• [88]Kishino H, Hasegawa M: Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J mol evol 1989, 29(2):170-179.
• [89]Gouret P, Paganini J, Dainat J, Louati D, Darbo E, Pontarotti P, Levasseur A: Integration of Evolutionary Biology Concepts for Functional Annotation and Automation of Complex Research in Evolution: The Multi-Agent Software System DAGOBAH. In Evolutionary Biology - Concepts, Biodiversity, Marcroevolution and Genome Evolution. Edited by Pontarotti P. Berlin Heidelberg: Springer - Verlag; 2011:71-76.
• [90]Lartillot N, Lepage T, Blanquart S: PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics (Oxford, England) 2009, 25(17):2286-2288.
• [91]Lartillot N, Philippe H: A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol biol evol 2004, 21(6):1095-1109.
• [92]Leplae R, Lima-Mendez G, Toussaint A: ACLAME: a CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res 2010, 38(Database issue):D57—61.
• [93]The Gene Ontology (GO) project in 2006 Nucleic acids res 2006, 34(Database issue):D322—326.
• [94]Zhou M, Cui Y: GeneInfoViz: constructing and visualizing gene relation networks. In silico biol 2004, 4(3):323-333.
• [95]Levasseur A, Paganini J, Dainat J, Thompson JD, Poch O, Pontarotti P, Gouret P: The chordate proteome history database. Evolutionary bioinf online 2012, 8:437-447.