Pathogen-origin horizontally transferred genes contribute to the evolution of Lepidopteran insects

BMC Evolutionary Biology

Ze Zhang²  Zhong-Huai Xiang¹  Yi-Hong Shen¹  Zi-Wen Li¹ 

[1] The Key Sericultural Laboratory of Agricultural Ministry, Southwest University, Chongqing 400715, China;The Institute of Agricultural and Life Sciences, Chongqing University, Chongqing 400044, China

关键词: Pathogenic bacteria;    Functional innovation;    Lepidoptera evolution;    Insect evolution;    Horizontal gene transfer;   

Others  :  1141926
DOI  :  10.1186/1471-2148-11-356

 received in 2011-05-13, accepted in 2011-12-12,  发布年份 2011

【 摘 要 】

Background

Horizontal gene transfer (HGT), a source of genetic variation, is generally considered to facilitate hosts' adaptability to environments. However, convincing evidence supporting the significant contribution of the transferred genes to the evolution of metazoan recipients is rare.

Results

In this study, based on sequence data accumulated to date, we used a unified method consisting of similarity search and phylogenetic analysis to detect horizontally transferred genes (HTGs) between prokaryotes and five insect species including Drosophila melanogaster, Anopheles gambiae, Bombyx mori, Tribolium castaneum and Apis mellifera. Unexpectedly, the candidate HTGs were not detected in D. melanogaster, An. gambiae and T. castaneum, and 79 genes in Ap. mellifera sieved by the same method were considered as contamination based on other information. Consequently, 14 types of 22 HTGs were detected only in the silkworm. Additionally, 13 types of the detected silkworm HTGs share homologous sequences in species of other Lepidopteran superfamilies, suggesting that the majority of these HTGs were derived from ancient transfer events before the radiation of Ditrysia clade. On the basis of phylogenetic topologies and BLAST search results, donor bacteria of these genes were inferred, respectively. At least half of the predicted donor organisms may be entomopathogenic bacteria. The predicted biochemical functions of these genes include four categories: glycosyl hydrolase family, oxidoreductase family, amino acid metabolism, and others.

Conclusions

The products of HTGs detected in this study may take part in comprehensive physiological metabolism. These genes potentially contributed to functional innovation and adaptability of Lepidopteran hosts in their ancient lineages associated with the diversification of angiosperms. Importantly, our results imply that pathogens may be advantageous to the subsistence and prosperity of hosts through effective HGT events at a large evolutionary scale.

【 授权许可】

   
2011 Li et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Duret L, Chureau C, Samain S, Weissenbach J, Avner P: The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 2006, 312(5780):1653-1655.
• [2]Choi IG, Kim SH: Global extent of horizontal gene transfer. Proc Natl Acad Sci USA 2007, 104(11):4489-4494.
• [3]Gilbert C, Schaack S, Pace JK, Brindley PJ, Feschotte C: A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 2010, 464(7293):1347-1350.
• [4]Kim DS, Lee Y, Hahn Y: Evidence for bacterial origin of heat shock RNA-1. RNA 2010, 16(2):274-279.
• [5]Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP: Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 2006, 38(8):953-956.
• [6]Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR: Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc Natl Acad Sci USA 2008, 105(46):17867-17871.
• [7]Schmitt I, Lumbsch HT: Ancient Horizontal Gene Transfer from Bacteria Enhances Biosynthetic Capabilities of Fungi. PLoS ONE 2009, 4(2):e4437.
• [8]Moran NA, Jarvik T: Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 2010, 328(5978):624-627.
• [9]Koonin EV, Makarova KS, Aravind L: Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 2001, 55:709-742.
• [10]Gogarten JP, Doolittle WF, Lawrence JG: Prokaryotic evolution in light of gene transfer. Mol Biol Evol 2002, 19(12):2226-2238.
• [11]Ochman H, Lawrence JG, Groisman EA: Lateral gene transfer and the nature of bacterial innovation. Nature 2000, 405(6784):299-304.
• [12]Garcia-Vallvé S, Romeu A, Palau J: Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res 2000, 10(11):1719-25.
• [13]Treangen TJ, Rocha EPC: Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 2011, 7(1):e1001284.
• [14]Andersson JO: Lateral gene transfer in eukaryotes. Cell Mol Life Sci 2005, 62:1182-1197.
• [15]Keeling PJ, Palmer JD: Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 2008, 9(8):605-618.
• [16]Yoshida S, Maruyama S, Nozaki H, Shirasu K: Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 2010, 328(5982):1128.
• [17]Dunning Hotopp JC: Horizontal gene transfer between bacteria and animals. Trends Genet 2011, 27(4):157-163.
• [18]Daimon T, Katsuma S, Iwanaga M, Kang WK, Shimada T: The BmChi-h gene, a bacterial-type chitinase gene of Bombyx mori, encodes a functional exochitinase that plays a role in the chitin degradation during the molting process. Insect Biochem Mol Biol 2005, 35(10):1112-1123.
• [19]Daimon T, Taguchi T, Meng Y, Katsuma S, Mita K, Shimada T: β-fructofuranosidase genes of the silkworm, Bombyx mori: insights into enzymatic adaptation of B. mori to toxic alkaloids in mulberry latex. J Biol Chem 2008, 283(22):15271-15279.
• [20]Meng Y, Katsuma S, Mita K, Shimada T: Abnormal red body coloration of the silkworm, Bombyx mori, is caused by a mutation in a novel kynureninase. Genes Cells 2009, 14(2):129-140.
• [21]Keeling PJ: Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr Opin Genet Dev 2009, 19(6):613-619.
• [22]Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Muñoz Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH: Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317(5845):1753-1756.
• [23]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.
• [24]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
• [25]Nikoh N, Nakabachi A: Aphids acquired symbiotic genes via lateral gene transfer. BMC Biology 2009, 7:12. BioMed Central Full Text
• [26]Nikoh N, McCutcheon JP, Kudo T, Miyagishima SY, Moran NA, Nakabachi A: Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 2010, 26(2):e1000827.
• [27]Mita K, Morimyo M, Okano K, Koike Y, Nohata J, Kawasaki H, Kadono-Okuda K, Yamamoto K, Suzuki MG, Shimada T, Goldsmith MR, Maeda S: The construction of an EST database for Bombyx mori and its application. Proc Natl Acad Sci USA 2003, 100(24):14121-14126.
• [28]Zhu B, Lou MM, Xie GL, Zhang GQ, Zhou XP, Li B, Jin GL: Horizontal gene transfer in silkworm, Bombyx mori. BMC Genomics 2011, 12:248. BioMed Central Full Text
• [29]Marcet-Houben M, Gabaldón T: Acquisition of prokaryotic genes by fungal genomes. Trends Genet 2010, 26(1):5-8.
• [30]Stanhope MJ, Lupas A, Italia MJ, Koretke KK, Volker C, Brown JR: Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 2001, 411(6840):940-944.
• [31]Salzberg SL, White O, Peterson J, Eisen JA: Microbial genes in the human genome: lateral transfer or gene loss? Science 2001, 292(5523):1903-1906.
• [32]Genereux DP, Logsdon JM Jr: Much ado about bacteria-to-vertebrate lateral gene transfer. Trends Genet 2003, 19(4):191-195.
• [33]Duan J, Li R, Cheng D, Fan W, Zha X, Cheng T, Wu Y, Wang J, Mita K, Xiang Z, Xia Q: SilkDB v2.0: a platform for silkworm (Bombyx mori) genome biology. Nucleic Acids Res 2010, 38(suppl 1):D453-D456.
• [34]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.
• [35]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
• [36]Felsenstein J: PHYLIP--Phylogeny Inference Package (Version 3.2). Cladistics 1989, 5:164-166.
• [37]Gascuel O: BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 1997, 14(7):685-695.
• [38]Higgins DG, Thompson JD, Gibson TJ: Using CLUSTAL for multiple sequence alignments. Methods Enzymol 1996, 226:383-402.
• [39]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24(8):1596-1599.
• [40]Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21(9):2104-2105.
• [41]Huelsenbeck JP, Ronquist F: MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 2001, 17(8):754-755.
• [42]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704.
• [43]The Nasonia Genome Working Group: Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 2010, 327(5963):343-348.
• [44]Munoz-Torres MC, Reese JT, Childers CP, Bennett AK, Sundaram JP, Childs KL, Anzola JM, Milshina N, Elsik CG: Hymenoptera Genome Database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res 2011, 39(suppl 1):D658-D662.
• [45]Xia Q, Cheng D, Duan J, Wang G, Cheng T, Zha X, Liu C, Zhao P, Dai F, Zhang Z, He N, Zhang L, Xiang Z: Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biol 2007, 8(8):R162. BioMed Central Full Text
• [46]Faulkner P: A hexose-l-phosphatase in silkworm blood. Biochem J 1955, 60(4):590-596.
• [47]Lee DC, Cottrill MA, Forsberg CW, Jia Z: Functional insights revealed by the crystal structures of Escherichia coli Glucose-1-phosphatase. J Biol Chem 2003, 278(33):31412-31418.
• [48]Shi L, Liu JF, An XM, Liang DC: Crystal structure of glycerophosphodiester phosphodiesterase (GDPD) from Thermoanaerobacter tengcongensis, a metal ion-dependent enzyme: Insight into the catalytic mechanism. Proteins 2008, 72(1):280-288.
• [49]Liu Y, Thoden JB, Kim J, Berger E, Gulick AM, Ruzicka FJ, Holden HM, Frey PA: Mechanistic roles of tyrosine 149 and serine 124 in UDP-galactose 4-epimerase from Escherichia coli. Biochemistry 1997, 36(35):10675-10684.
• [50]Ilari A, Bonamore A, Franceschini S, Fiorillo A, Boffi A, Colotti G: The X-ray structure of N-methyltryptophan oxidase reveals the structural determinants of substrate specificity. Proteins 2008, 71(4):2065-2075.
• [51]Thorn JM, Barton JD, Dixon NE, Ollis DL, Edwards KJ: Crystal structure of Escherichia coli QOR quinone oxidoreductase complexed with NADPH. J Mol Biol 1995, 249(4):785-799.
• [52]Shimomura Y, Kakuta Y, Fukuyama K: Crystal structures of the quinone oxidoreductase from Thermus thermophilus HB8 and its complex with NADPH: implication for NADPH and substrate recognition. J Bacteriol 2003, 185(14):4211-4218.
• [53]Pauchet Y, Wilkinson P, Vogel H, Nelson DR, Reynolds SE, Heckel DG, ffrench-Constant RH: Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol Biol 2010, 19(1):61-75.
• [54]Papanicolaou A, Gebauer-Jung S, Blaxter ML, Owen McMillan W, Jiggins CD: ButterflyBase: a platform for lepidopteran genomics. Nucl Acids Res 2008, 36(suppl 1):D582-D587.
• [55]Regier JC, Zwick A, Cummings MP, Kawahara AY, Cho S, Weller S, Roe A, Baixeras J, Brown JW, Parr C, Davis DR, Epstein M, Hallwachs W, Hausmann A, Janzen DH, Kitching IJ, Solis MA, Yen SH, Bazinet AL, Mitter C: Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC Evol Biol 2009, 9:280. BioMed Central Full Text
• [56]Grimont PAD, Grimont F: The Genus Serratia. Annu Rev Microbiol 1978, 32:221-248.
• [57]Jander G, Rahme LG, Ausubel FM: Positive Correlation between Virulence of Pseudomonas aeruginosa Mutants in Mice and Insects. J Bacteriol 2000, 182(13):3843-3845.
• [58]Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV: Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 2000, 406(6799):959-964.
• [59]Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Givaudan A, Taourit S, Bocs S, Boursaux-Eude C, Chandler M, Charles JF, Dassa E, Derose R, Derzelle S, Freyssinet G, Gaudriault S, Médigue C, Lanois A, Powell K, Siguier P, Vincent R, Wingate V, Zouine M, Glaser P, Boemare N, Danchin A, Kunst F: The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat Biotechnol 2003, 21(11):1307-1313.
• [60]Vallet-Gely I, Lemaitre B, Boccard F: Bacterial strategies to overcome insect defences. Nat Rev Microbiol 2008, 6(4):302-313.
• [61]Wilkinson P, Waterfield NR, Crossman L, Corton C, Sanchez-Contreras M, Vlisidou I, Barron A, Bignell A, Clark L, Ormond D, Mayho M, Bason N, Smith F, Simmonds M, Churcher C, Harris D, Thompson NR, Quail M, Parkhill J, Ffrench-Constant RH: Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens. BMC Genomics 2009, 10:302. BioMed Central Full Text
• [62]Gaspar F, Teixeira N, Rigottier-Gois L, Marujo P, Nielsen-LeRoux C, Crespo MT, Lopes Mde F, Serror P: Virulence of Enterococcus faecalis dairy strains in an insect model: the role of fsrB and gelE. Microbiology 2009, 155(Pt 11):3564-3571.
• [63]Hanin A, Sava I, Bao Y, Huebner J, Hartke A, Auffray Y, Sauvageot N: Screening of in vivo activated genes in Enterococcus faecalis during insect and mouse infections and growth in urine. PLoS One 2010, 5(7):e11879.
• [64]Corpe WA, Rheem S: Ecology of the methylotrophic bacteria on living leaf surfaces. FEMS Microbiol Ecol 1989, 62:243-250.
• [65]Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA: Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA 2009, 106(38):16428-16433.
• [66]Werren JH, Windsor DM: Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc Biol Sci 2000, 267(1450):1277-1285.
• [67]Fenn K, Conlon C, Jones M, Quail MA, Holroyd NE, Parkhill J, Blaxter M: Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathog 2006, 2(10):e94.
• [68]Korochkina S, Barreau C, Pradel G, Jeffery E, Li J, Natarajan R, Shabanowitz J, Hunt D, Frevert U, Vernick KD: A mosquito-specific protein family includes candidate receptors for malaria sporozoite invasion of salivary glands. Cell Microbiol 2006, 8(1):163-175.
• [69]Woolfit M, Iturbe-Ormaetxe I, McGraw EA, O'Neill SL: An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol Biol Evol 2009, 26(2):367-374.
• [70]Nosenko T, Bhattacharya D: Horizontal gene transfer in chromalveolates. BMC Evol Biol 2007, 7:173. BioMed Central Full Text
• [71]The International Aphid Genomics Consortium: Genome Sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biol 2010, 8(2):e1000313.
• [72]Corderoand OX, Hogeweg P: The impact of long-distance horizontal gene transfer on prokaryotic genome size. Proc Natl Acad Sci USA 2009, 106(51):21748-21753.
• [73]Lawrence JG, Ochman H: Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 1997, 44:383-397.
• [74]Hooper SD, Berg OG: Duplication is more common among laterally transferred genes than among indigenous genes. Genome Biol 2003, 4(8):R48. BioMed Central Full Text
• [75]Puttaraju HP, Madhu M: Presence of Wolbachia endosymbionts in different silkworm species and races and in their uzi fly parasites. J Invertebr Pathol 2002, 79(2):120-122.
• [76]McNulty SN, Foster JM, Mitreva M, Dunning Hotopp JC, Martin J, Fischer K, Wu B, Davis PJ, Kumar S, Brattig NW, Slatko BE, Weil GJ, Fischer PU: Endosymbiont DNA in endobacteria-free filaria nematodes indicates ancient horizontal genetic transfer. PLoS ONE 2010, 5(6):e11029.
• [77]Grimaldi D, Engel MS: Evolution of the insects. Cambridge University Press; 2005.
• [78]Ochman H, Moran NA: Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 2001, 292(5519):1096-1099.
• [79]van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, Fernández JM, Jiménez L, Postigo M, Silva FJ, Tamames J, Viguera E, Latorre A, Valencia A, Morán F, Moya A: Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci USA 2003, 100(2):581-586.
• [80]Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M: The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 2006, 314(5797):267.
• [81]Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H: Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 2000, 407(6800):81-86.
• [82]Tamas I, Klasson L, Canbäck B, Näslund AK, Eriksson AS, Wernegreen JJ, Sandström JP, Moran NA, Andersson SG: 50 million years of genomic stasis in endosymbiotic bacteria. Science 2002, 296(5577):2376-2379.
• [83]Blaxter M: Symbiont genes in host genomes: fragments with a future? Cell Host Microbe 2007, 2(4):211-213.