| Genome Biology | |
| Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes | |
| Robert P Hirt2  T Martin Embley2  Sirintra Nakjang2  Thomas Sicheritz-Ponten1  Peter G Foster3  Cecilia Alsmark4  | |
| [1] Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, DK-2800 Lyngby and Novo Nordisk Foundation Center for Biosustainability, DK-2900 Hørsholm, Denmark;Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK;Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK;Division of Pharmacognosy, Department of Medicinal Chemistry, Uppsala University, Biomedical Centre, S-751 23 Uppsala, Sweden | |
| 关键词: parasites; eukaryotes; lateral gene transfer; phylogenomics; Genome evolution; | |
| Others : 1136535 DOI : 10.1186/gb-2013-14-2-r19 |
|
| received in 2012-10-18, accepted in 2013-02-25, 发布年份 2013 | |
PDF
|
|
【 摘 要 】
Background
The influence of lateral gene transfer on gene origins and biology in eukaryotes is poorly understood compared with those of prokaryotes. A number of independent investigations focusing on specific genes, individual genomes, or specific functional categories from various eukaryotes have indicated that lateral gene transfer does indeed affect eukaryotic genomes. However, the lack of common methodology and criteria in these studies makes it difficult to assess the general importance and influence of lateral gene transfer on eukaryotic genome evolution.
Results
We used a phylogenomic approach to systematically investigate lateral gene transfer affecting the proteomes of thirteen, mainly parasitic, microbial eukaryotes, representing four of the six eukaryotic super-groups. All of the genomes investigated have been significantly affected by prokaryote-to-eukaryote lateral gene transfers, dramatically affecting the enzymes of core pathways, particularly amino acid and sugar metabolism, but also providing new genes of potential adaptive significance in the life of parasites. A broad range of prokaryotic donors is involved in such transfers, but there is clear and significant enrichment for bacterial groups that share the same habitats, including the human microbiota, as the parasites investigated.
Conclusions
Our data show that ecology and lifestyle strongly influence gene origins and opportunities for gene transfer and reveal that, although the outlines of the core eukaryotic metabolism are conserved among lineages, the genes making up those pathways can have very different origins in different eukaryotes. Thus, from the perspective of the effects of lateral gene transfer on individual gene ancestries in different lineages, eukaryotic metabolism appears to be chimeric.
【 授权许可】
2013 Alsmark et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
|---|---|---|---|
| 20150313031701174.pdf | 1064KB | ||
| Figure 5. | 78KB | Image | |
| Figure 4. | 16KB | Image | |
| Figure 3. | 83KB | Image | |
| Figure 2. | 127KB | Image | |
| Figure 1. | 66KB | Image |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
【 参考文献 】
- [1]Kaessmann H: Origins, evolution, and phenotypic impact of new genes. Genome Res 2010, 20:1313-1326.
- [2]Zmasek CM, Godzik A: Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires. Genome Biol 2011, 12:R4. BioMed Central Full Text
- [3]Zhaxybayeva O, Doolittle WF: Lateral gene transfer. Curr Biol 2011, 21:R242-246.
- [4]Gogarten JP, Townsend JP: Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 2005, 3:679-687.
- [5]Andersson JO: Gene transfer and diversification of microbial eukaryotes. Annu Rev Microbiol 2009, 63:177-193.
- [6]Keeling PJ: Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr Opin Genet Dev 2009, 19:613-619.
- [7]Keeling PJ, Palmer JD: Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 2008, 9:605-618.
- [8]Jain R, Rivera MC, Lake JA: Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA 1999, 96:3801-3806.
- [9]Esser C, Ahmadinejad N, Wiegand C, Rotte C, Sebastiani F, Gelius-Dietrich G, Henze K, Kretschmann E, Richly E, Leister D, Bryant D, Steel MA, Lockhart PJ, Penny D, Martin W: A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol 2004, 21:1643-1660.
- [10]Embley TM, Martin W: Eukaryotic evolution, changes and challenges. Nature 2006, 440:623-630.
- [11]Thiergart T, Landan G, Schenk M, Dagan T, Martin WF: An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biol Evol 2012, 4:466-485.
- [12]Timmis JN, Ayliffe MA, Huang CY, Martin W: Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 2004, 5:123-135.
- [13]Gabaldon T, Huynen MA: From endosymbiont to host-controlled organelle: the hijacking of mitochondrial protein synthesis and metabolism. PLoS Comput Biol 2007, 3:e219.
- [14]Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, Moule S, Mungall K, Ormond D, et al.: The genome of the protist parasite Entamoeba histolytica. Nature 2005, 433:865-868.
- [15]Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL, Alsmark UC, Besteiro S, Sicheritz-Ponten T, Noel CJ, Dacks JB, Foster PG, Simillion C, Van de Peer Y, Miranda-Saavedra D, Barton GJ, Westrop GD, Muller S, Dessi D, Fiori PL, Ren Q, Paulsen I, Zhang H, Bastida-Corcuera FD, Simoes-Barbosa A, Brown MT, Hayes RD, Mukherjee M, et al.: Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 2007, 315:207-212.
- [16]Whitaker JW, McConkey GA, Westhead DR: The transferome of metabolic genes explored: analysis of the horizontal transfer of enzyme encoding genes in unicellular eukaryotes. Genome Biol 2009, 10:R36. BioMed Central Full Text
- [17]Tsaousis AD, Kunji ER, Goldberg AV, Lucocq JM, Hirt RP, Embley TM: A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 2008, 453:553-556.
- [18]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, 38:953-956.
- [19]Ragan MA: On surrogate methods for detecting lateral gene transfer. FEMS Microbiol Lett 2001, 201:187-191.
- [20]Schmidt GD, Roberts LS: Foundations of parasitology. 8th edition. New York: McGraw-Hill; 2009.
- [21]Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, et al.: The genome of the social amoeba Dictyostelium discoideum. Nature 2005, 435:43-57.
- [22]Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Bohme U, Hannick L, Aslett MA, Shallom J, Marcello L, Hou L, Wickstead B, Alsmark UC, Arrowsmith C, Atkin RJ, Barron AJ, Bringaud F, Brooks K, Carrington M, Cherevach I, Chillingworth TJ, Churcher C, Clark LN, Corton CH, Cronin A, et al.: The genome of the African trypanosome Trypanosoma brucei. Science 2005, 309:416-422.
- [23]Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, Quail MA, Peters N, Adlem E, Tivey A, Aslett M, Kerhornou A, Ivens A, Fraser A, Rajandream MA, Carver T, Norbertczak H, Chillingworth T, Hance Z, Jagels K, Moule S, Ormond D, Rutter S, Squares R, Whitehead S, Rabbinowitsch E, Arrowsmith C, White B, Thurston S, Bringaud F, Baldauf SL, et al.: Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 2007, 39:839-847.
- [24]Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, Davids BJ, Dawson SC, Elmendorf HG, Hehl AB, Holder ME, Huse SM, Kim UU, Lasek-Nesselquist E, Manning G, Nigam A, Nixon JE, Palm D, Passamaneck NE, Prabhu A, Reich CI, Reiner DS, Samuelson J, Svard SG, Sogin ML: Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 2007, 317:1921-1926.
- [25]Huang J, Mullapudi N, Sicheritz-Ponten T, Kissinger JC: A first glimpse into the pattern and scale of gene transfer in Apicomplexa. Int J Parasitol 2004, 34:265-274.
- [26]Huang J, Mullapudi N, Lancto CA, Scott M, Abrahamsen MS, Kissinger JC: Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol 2004, 5:R88. BioMed Central Full Text
- [27]Doolittle WF: You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 1998, 14:307-311.
- [28]Brock DA, Douglas TE, Queller DC, Strassmann JE: Primitive agriculture in a social amoeba. Nature 2011, 469:393-396.
- [29]Rendon-Maldonado JG, Espinosa-Cantellano M, Gonzalez-Robles A, Martinez-Palomo A: Trichomonas vaginalis: in vitro phagocytosis of lactobacilli, vaginal epithelial cells, leukocytes, and erythrocytes. Exp Parasitol 1998, 89:241-250.
- [30]Sekirov I, Russell SL, Antunes LC, Finlay BB: Gut microbiota in health and disease. Physiol Rev 2010, 90:859-904.
- [31]McGuckin MA, Linden SK, Sutton P, Florin TH: Mucin dynamics and enteric pathogens. Nat Rev Microbiol 2011, 9:265-278.
- [32]Wiggins R, Hicks SJ, Soothill PW, Millar MR, Corfield AP: Mucinases and sialidases: their role in the pathogenesis of sexually transmitted infections in the female genital tract. Sex Transm Infect 2001, 77:402-408.
- [33]de Koning AP, Brinkman FS, Jones SJ, Keeling PJ: Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis. Mol Biol Evol 2000, 17:1769-1773.
- [34]Koropatkin NM, Cameron EA, Martens EC: How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 2012, 10:323-335.
- [35]Yoshida N, Camargo EP: Ureotelism and ammonotelism in trypanosomatids. J Bacteriol 1978, 136:1184-1186.
- [36]Opperdoes FR, Coombs GH: Metabolism of Leishmania: proven and predicted. Trends Parasitol 2007, 23:149-158.
- [37]McConville MJ, de Souza D, Saunders E, Likic VA, Naderer T: Living in a phagolysosome; metabolism of Leishmania amastigotes. Trends Parasitol 2007, 23:368-375.
- [38]Schlein Y, Borut S, Greenblatt CL: Development of sandfly forms of Leishmania major in sucrose solutions. J Parasitol 1987, 73:797-805.
- [39]Gontijo NF, Melo MN, Riani EB, Almeida-Silva S, Mares-Guia ML: Glycosidases in Leishmania and their importance for Leishmania in phlebotomine sandflies with special reference to purification and characterization of a sucrase. Exp Parasitol 1996, 83:117-124.
- [40]Eschenlauer SC, Faria MS, Morrison LS, Bland N, Ribeiro-Gomes FL, DosReis GA, Coombs GH, Lima AP, Mottram JC: Influence of parasite encoded inhibitors of serine peptidases in early infection of macrophages with Leishmania major. Cell Microbiol 2009, 11:106-120.
- [41]Muller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, van der Giezen M, Tielens AG, Martin WF: Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 2012, 76:444-495.
- [42]Zuo X, Coombs GH: Amino acid consumption by the parasitic, amoeboid protists Entamoeba histolytica and E. invadens. FEMS Microbiol Lett 1995, 130:253-258.
- [43]Zuo X, Lockwood BC, Coombs GH: Uptake of amino acids by the parasitic, flagellated protist Trichomonas vaginalis. Microbiology 1995, 141:2637-2642.
- [44]Anderson IJ, Loftus BJ: Entamoeba histolytica: observations on metabolism based on the genome sequence. Exp Parasitol 2005, 110:173-177.
- [45]Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI: Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 2008, 6:776-788.
- [46]Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, et al.: A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65.
- [47]Consortium HMP: Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214.
- [48]Cribby S, Taylor M, Reid G: Vaginal microbiota and the use of probiotics. Interdiscip Perspect Infect Dis 2008, 2008:256490.
- [49]Gimenez G, Bertelli C, Moliner C, Robert C, Raoult D, Fournier PE, Greub G: Insight into cross-talk between intra-amoebal pathogens. BMC Genomics 2011, 12:542. BioMed Central Full Text
- [50]Nakamura Y, Itoh T, Matsuda H, Gojobori T: Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat Genet 2004, 36:760-766.
- [51]Chan CX, Beiko RG, Darling AE, Ragan MA: Lateral transfer of genes and gene fragments in prokaryotes. Genome Biol Evol 2009, 1:429-438.
- [52]Noel CJ, Diaz N, Sicheritz-Ponten T, Safarikova L, Tachezy J, Tang P, Fiori PL, Hirt RP: Trichomonas vaginalis vast BspA-like gene family: evidence for functional diversity from structural organisation and transcriptomics. BMC Genomics 2010, 11:99. BioMed Central Full Text
- [53]Nakjang S, Ndeh DA, Wipat A, Bolam DN, Hirt RP: A novel extracellular metallopeptidase domain shared by animal host-associated mutualistic and pathogenic microbes. PLoS ONE 2012, 7:e30287.
- [54]Clark EA, Walker N, Ford DC, Cooper IA, Oyston PC, Acharya KR: Molecular recognition of chymotrypsin by the serine protease inhibitor ecotin from Yersinia pestis. J Biol Chem 2011, 286:24015-24022.
- [55]Connaris S, Greenwell P: Glycosidases in mucin-dwelling protozoans. Glycoconj J 1997, 14:879-882.
- [56]Lockwood BC, North MJ, Coombs GH: The release of hydrolases from Trichomonas vaginalis and Tritrichomonas foetus. Mol Biochem Parasitol 1988, 30:135-142.
- [57]Loiseau PM, Bories C, Sanon A: The chitinase system from Trichomonas vaginalis as a potential target for antimicrobial therapy of urogenital trichomoniasis. Biomed Pharmacother 2002, 56:503-510.
- [58]Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ: Ecology drives a global network of gene exchange connecting the human microbiome. Nature 2011, 480:241-244.
- [59]Umejiego NN, Gollapalli D, Sharling L, Volftsun A, Lu J, Benjamin NN, Stroupe AH, Riera TV, Striepen B, Hedstrom L: Targeting a prokaryotic protein in a eukaryotic pathogen: identification of lead compounds against cryptosporidiosis. Chem Biol 2008, 15:70-77.
- [60]Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, E NS, R SH, Awono-Ambene PH, Levashina EA, Christen R, Morlais I: Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathogens 2012, 8:e1002742.
- [61]Lindh JM, Lehane MJ: The tsetse fly Glossina fuscipes fuscipes (Diptera: Glossina) harbours a surprising diversity of bacteria other than symbionts. Antonie van Leeuwenhoek 2011, 99:711-720.
- [62]Weiss B, Aksoy S: Microbiome influences on insect host vector competence. Trends Parasitol 2011, 27:514-522.
- [63]Ni T, Yue J, Sun G, Zou Y, Wen J, Huang J: Ancient gene transfer from algae to animals: Mechanisms and evolutionary significance. BMC Evol Biol 2012, 12:83. BioMed Central Full Text
- [64]SpyPhy [http://www.cbs.dtu.dk/staff/thomas/pyphy/spyphy.html] webcite
- [65]Altschul SF, Madden TL, Schaffer 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, 25:3389-3402.
- [66]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, 22:4673-4680.
- [67]Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552.
- [68]Swofford DL: PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts; 2003.
- [69]Nair R, Rost B: Inferring sub-cellular localization through automated lexical analysis. Bioinformatics 2002, 18 Suppl 1:S78-86.
- [70]Rost B: Twilight zone of protein sequence alignments. Protein Eng 1999, 12:85-94.
- [71]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
- [72]Cummings MP, Handley SA, Myers DS, Reed DL, Rokas A, Winka K: Comparing bootstrap and posterior probability values in the four-taxon case. Syst Biol 2003, 52:477-487.
- [73]Foster PG: Modeling compositional heterogeneity. Syst Biol 2004, 53:485-495.
- [74]Desper R, Gascuel O: Theoretical foundation of the balanced minimum evolution method of phylogenetic inference and its relationship to weighted least-squares tree fitting. Mol Biol Evol 2004, 21:587-598.
- [75]Douady CJ, Delsuc F, Boucher Y, Doolittle WF, Douzery EJ: Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol Biol Evol 2003, 20:248-254.
- [76]Kanehisa M, Goto S: KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28:27-30.
- [77]Sjolander K: Phylogenomic inference of protein molecular function: advances and challenges. Bioinformatics 2004, 20:170-179.
- [78]Yamada T, Letunic I, Okuda S, Kanehisa M, Bork P: iPath2.0: interactive pathway explorer. Nucleic Acids Res 2011, 39:W412-415.
- [79]Brockhausen I, Schachter H, Stanley P: O-GalNAc Glycans. In Essentials of Glycobiology. 2nd edition. Edited by Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2009:115-128.
- [80]Wasmuth J, Daub J, Peregrin-Alvarez JM, Finney CA, Parkinson J: The origins of apicomplexan sequence innovation. Genome Res 2009, 19:1202-1213.
- [81]Wilkinson M, McInerney JO, Hirt RP, Foster PG, Embley TM: Of clades and clans: terms for phylogenetic relationships in unrooted trees. Trends Ecol Evol 2007, 22:114-115.
PDF