The scale and evolutionary significance of horizontal gene transfer in the choanoflagellate Monosiga brevicollis

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Yue, Jipei ^a,b   Sun, Guiling ^a,b   Hu, Xiangyang ^a   Huang, Jinling ^b  

^a KUNMING INSTITUTE OF BOTANY   (China)

^b EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Adaptation; Choanoflagellates; Eukaryotic evolution; Genome evolution; HGT frequency

Indexed keywords

ASCORBIC ACID; PHOSPHOLIPID; PORPHYRIN; VITAMIN K GROUP;

AMINO ACID METABOLISM; ARTICLE; CARBOHYDRATE METABOLISM; CHEMICAL STRESS; ENDOSYMBIONT; EVOLUTION; GENE IDENTIFICATION; HORIZONTAL GENE TRANSFER; MONOSIGA BREVICOLLIS; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PHYLOGENOMICS; PLASTID; BACTERIA; CHOANOFLAGELLATE; CLASSIFICATION; GENETIC DATABASE; GENETICS; GENOME; GREEN ALGA; PHYLOGENY;

ALGAE; ANIMALIA; CHOANOFLAGELLIDA; EUKARYOTA; MONOSIGA; MONOSIGA BREVICOLLIS; PROKARYOTA; PROTISTA;

BACTERIA; BIOLOGICAL EVOLUTION; CHLOROPHYTA; CHOANOFLAGELLATA; DATABASES, GENETIC; GENE TRANSFER, HORIZONTAL; GENOME, PROTOZOAN; PHYLOGENY;

EID: 84886744552     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-729     Document Type: Article

References (79)

1. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature 2000, 405(6784):299-304. 10.1038/35012500, 10830951.
2. Gogarten JP, Doolittle WF, Lawrence JG. Prokaryotic evolution in light of gene transfer. Mol Biol Evol 2002, 19(12):2226-2238. 10.1093/oxfordjournals.molbev.a004046, 12446813.
3. Andersson JO. Lateral gene transfer in eukaryotes. Cell Mol Life Sci 2005, 62(11):1182-1197. 10.1007/s00018-005-4539-z, 15761667.
4. Keeling PJ, Palmer JD. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 2008, 9(8):605-618. 10.1038/nrg2386, 18591983.
5. Doolittle WF. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 1998, 14(8):307-311. 10.1016/S0168-9525(98)01494-2, 9724962.
6. Nixon JE, Wang A, Field J, Morrison HG, McArthur AG, Sogin ML, Loftus BJ, Samuelson J. Evidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase, and alcohol dehydrogenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica. Eukaryot Cell 2002, 1(2):181-190. 10.1128/EC.1.2.181-190.2002, 118039, 12455953.
7. Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc Natl Acad Sci USA 2003, 100(13):7678-7683. 10.1073/pnas.1230951100, 164647, 12777624.
8. Andersson JO, Sjogren AM, Davis LA, Embley TM, Roger AJ. Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 2003, 13(2):94-104. 10.1016/S0960-9822(03)00003-4, 12546782.
9. Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, et al. The genome of the protist parasite Entamoeba histolytica. Nature 2005, 433(7028):865-868. 10.1038/nature03291, 15729342.
10. Leadbeater BSC, Kelly M. Evolution of animals' choanoflagellates and sponges. Water Atmosph Online 2001, 9(2):9-11.
11. Carr M, Leadbeater BS, Hassan R, Nelson M, Baldauf SL. Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc Natl Acad Sci USA 2008, 105(43):16641-16646. 10.1073/pnas.0801667105, 2575473, 18922774.
12. Lavrov DV, Forget L, Kelly M, Lang BF. Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution. Mol Biol Evol 2005, 22(5):1231-1239. 10.1093/molbev/msi108, 15703239.
13. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008, 451(7180):783-788. 10.1038/nature06617, 2562698, 18273011.
14. Leakey RJG, Leadbeater BSC, Mitchell E, McCready SMM, Murray AWA. The abundance and biomass of choanoflagellates and other nanoflagellates in waters of contrasting temperature to the north-west of South Georgia in the Southern Ocean. Eur J Protistol 2002, 38(4):333-350.
15. Nedelcu AM, Miles IH, Fagir AM, Karol K. Adaptive eukaryote-to-eukaryote lateral gene transfer: stress-related genes of algal origin in the closest unicellular relatives of animals. J Evol Biol 2008, 21(6):1852-1860. 10.1111/j.1420-9101.2008.01605.x, 18717747.
16. Sun G, Yang Z, Ishwar A, Huang J. Algal genes in the closest relatives of animals. Mol Biol Evol 2010, 27(12):2879-2889. 10.1093/molbev/msq175, 20627874.
17. Tucker RP, Beckmann J, Leachman NT, Scholer J, Chiquet-Ehrismann R. Phylogenetic analysis of the teneurins: conserved features and premetazoan ancestry. Mol Biol Evol 2012, 29(3):1019-1029. 10.1093/molbev/msr271, 3278476, 22045996.
18. Foerstner KU, Doerks T, Muller J, Raes J, Bork P. A nitrile hydratase in the eukaryote Monosiga brevicollis. PloS one 2008, 3(12):e3976. 10.1371/journal.pone.0003976, 2603476, 19096720.
19. Frickey T, Lupas AN. PhyloGenie: automated phylome generation and analysis. Nucleic Acids Res 2004, 32(17):5231-5238. 10.1093/nar/gkh867, 521674, 15459293.
20. Podell S, Gaasterland T. DarkHorse: a method for genome-wide prediction of horizontal gene transfer. Genome Biol 2007, 8(2):R16. 10.1186/gb-2007-8-2-r16, 1852411, 17274820.
21. Tian J, Sun G, Ding Q, Huang J, Oruganti S, Xie B. AlienG: an effective computational tool for phylogenetic identification of horizontally transferred genes 2011, New Orleans, Louisiana: The third International Conference on Bioinformatics and Computational Biology (BICoB).
22. Hackett JD, Yoon HS, Li S, Reyes-Prieto A, Rummele SE, Bhattacharya D. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol Biol Evol 2007, 24(8):1702-1713. 10.1093/molbev/msm089, 17488740.
23. Huang J, Gogarten JP. Ancient horizontal gene transfer can benefit phylogenetic reconstruction. Trends Genet 2006, 22(7):361-366. 10.1016/j.tig.2006.05.004, 16730850.
24. Huang J, Gogarten JP. Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids?. Genome Biol 2007, 8(6):R99. 10.1186/gb-2007-8-6-r99, 2394758, 17547748.
25. Li S, Nosenko T, Hackett JD, Bhattacharya D. Phylogenomic analysis identifies red algal genes of endosymbiotic origin in the chromalveolates. Mol Biol Evol 2006, 23(3):663-674.
26. Podell S, Gaasterland T, Allen EE. A database of phylogenetically atypical genes in archaeal and bacterial genomes, identified using the DarkHorse algorithm. BMC Bioinform 2008, 9:419.
27. Zhaxybayeva O, Swithers KS, Lapierre P, Fournier GP, Bickhart DM, DeBoy RT, Nelson KE, Nesbo CL, Doolittle WF, Gogarten JP, et al. On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales. Proc Natl Acad Sci USA 2009, 106(14):5865-5870. 10.1073/pnas.0901260106, 2667022, 19307556.
28. Sun G, Yang Z, Kosch T, Summers K, Huang J. Evidence for acquisition of virulence effectors in pathogenic chytrids. BMC Evol Biol 2011, 11:195. 10.1186/1471-2148-11-195, 3161006, 21740557.
29. 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(1):83. 10.1186/1471-2148-12-83, 3494510, 22690978.
30. Yue J, Hu X, Sun H, Yang Y, Huang J. Widespread impact of horizontal gene transfer on plant colonization of land. Nat Commun 2012, 3:1152. 3493653, 23093189.
31. Sun G, Huang J. Horizontally acquired DAP pathway as a unit of self-regulation. J Evol Biol 2011, 24(3):587-595. 10.1111/j.1420-9101.2010.02192.x, 21159005.
32. Kurland CG, Canback B, Berg OG. Horizontal gene transfer: a critical view. P Natl Acad Sci USA 2003, 100(17):9658-9662.
33. Stiller JW. Experimental design and statistical rigor in phylogenomics of horizontal and endosymbiotic gene transfer. BMC Evol Biol 2011, 11:259. 10.1186/1471-2148-11-259, 3190393, 21923904.
34. Stiller JW, Huang J, Ding Q, Tian J, Goodwillie C. Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses?. BMC genomics 2009, 10:484. 10.1186/1471-2164-10-484, 2770532, 19843329.
35. Keeling PJ. Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol 2009, 56(1):1-8. 10.1111/j.1550-7408.2008.00371.x, 19335769.
36. Buck KR, Chavez FP, Thomsen HA. Choanoflagellates of the central California waters: abundance and distribution. Ophelia 1991, 33(3):179-186.
37. Marchant H, Scott F. Uptake of sub-micrometre particles and dissolved organic material by Antarctic choanoflagellates. Mar Ecol Prog Ser 1993, 92:59-64.
38. Flynn KJ, Stoecker DK, Mitra A, Raven JA, Glibert PM, Hansen PJ, Granéli E, Burkholder JM. Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J Plankton Res 2013, 35(1):3-11.
39. Raven JA, Beardall J, Flynn KJ, Maberly SC. Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin's insectivorous plants. J Exp Bot 2009, 60(14):3975-3987. 10.1093/jxb/erp282, 19767306.
40. Huang JL, Mullapudi N, Sicheritz-Ponten T, Kissinger JC. A first glimpse into the pattern and scale of gene transfer in the Apicomplexa. Int J Parasitol 2004, 34(3):265-274. 10.1016/j.ijpara.2003.11.025, 15003488.
41. Hackett JD, Yoon HS, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Nosenko T, Bhattacharya D. Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr Biol 2004, 14(3):213-218.
42. Dagan T, Martin W. Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution. Proc Natl Acad Sci USA 2007, 104(3):870-875. 10.1073/pnas.0606318104, 1783406, 17213324.
43. Alsmark UC, Sicheritz-Ponten T, Foster PG, Hirt RP, Embley TM. Horizontal gene transfer in eukaryotic parasites: a case study of Entamoeba histolytica and Trichomonas vaginalis. Methods Mol Biol (Clifton, NJ) 2009, 532:489-500.
44. Andersson JO. Evolution of patchily distributed proteins shared between eukaryotes and prokaryotes: Dictyostelium as a case study. J Mol Microbiol Biotechnol 2011, 20(2):83-95. 10.1159/000324505, 21430389.
45. Schonknecht G, Chen WH, Ternes CM, Barbier GG, Shrestha RP, Stanke M, Brautigam A, Baker BJ, Banfield JF, Garavito RM, et al. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science (New York, NY) 2013, 339(6124):1207-1210.
46. Boschetti C, Carr A, Crisp A, Eyres I, Wang-Koh Y, Lubzens E, Barraclough TG, Micklem G, Tunnacliffe A. Biochemical diversification through foreign gene expression in Bdelloid rotifers. PLoS Gen 2012, 8(11):e1003035.
47. Gogarten JP, Townsend JP. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 2005, 3(9):679-687. 10.1038/nrmicro1204, 16138096.
48. Andersson JO, Sjogren AM, Horner DS, Murphy CA, Dyal PL, Svard SG, Logsdon JM, Ragan MA, Hirt RP, Roger AJ. A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution. BMC genomics 2007, 8:51. 10.1186/1471-2164-8-51, 1805757, 17298675.
49. Nedelcu AM, Blakney AJ, Logue KD. Functional replacement of a primary metabolic pathway via multiple independent eukaryote-to-eukaryote gene transfers and selective retention. J Evol Biol 2009, 22(9):1882-1894. 10.1111/j.1420-9101.2009.01797.x, 19619164.
50. Garcia-Vallve S, Romeu A, Palau J. Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol Biol Evol 2000, 17(3):352-361. 10.1093/oxfordjournals.molbev.a026315, 10723736.
51. Ricard G, McEwan NR, Dutilh BE, Jouany JP, Macheboeuf D, Mitsumori M, McIntosh FM, Michalowski T, Nagamine T, Nelson N, et al. Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC genomics 2006, 7:22. 10.1186/1471-2164-7-22, 1413528, 16472398.
52. Sies H. Oxidative stress: oxidants and antioxidants. Exp Physiol 1997, 82(2):291-295.
53. Vertuani S, Angusti A, Manfredini S. The antioxidants and pro-antioxidants network: an overview. Curr Pharm Des 2004, 10(14):1677-1694. 10.2174/1381612043384655, 15134565.
54. Conter A, Gangneux C, Suzanne M, Gutierrez C. Survival of Escherichia coli during long-term starvation: effects of aeration, NaCl, and the rpoS and osmC gene products. Res Microbiol 2001, 152(1):17-26. 10.1016/S0923-2508(00)01164-5, 11281321.
55. Lee J, Spector D, Godon C, Labarre J, Toledano MB. A new antioxidant with alkyl hydroperoxide defense properties in yeast. J Biol Chem 1999, 274(8):4537-4544. 10.1074/jbc.274.8.4537, 9988687.
56. Leterrier M, Corpas FJ, Barroso JB, Sandalio LM, del Rio LA. Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 2005, 138(4):2111-2123. 10.1104/pp.105.066225, 1183399, 16055677.
57. Pineau B, Layoune O, Danon A, De Paepe R. L-galactono-1,4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. J Biol Chem 2008, 283(47):32500-32505. 10.1074/jbc.M805320200, 18799460.
58. Teixeira FK, Menezes-Benavente L, Margis R, Margis-Pinheiro M. Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: inferences from the rice genome. J Mol Evol 2004, 59(6):761-770. 10.1007/s00239-004-2666-z, 15599508.
59. Gronlien HK, Berg T, Lovlie AM. In the polymorphic ciliate Tetrahymena vorax, the non-selective phagocytosis seen in microstomes changes to a highly selective process in macrostomes. J Exp Biol 2002, 205(Pt 14):2089-2097.
60. Miura N, Ishida N, Hoshino M, Yamauchi M, Hara T, Ayusawa D, Kawakita M. Human UDP-galactose translocator: molecular cloning of a complementary DNA that complements the genetic defect of a mutant cell line deficient in UDP-galactose translocator. J Biochem 1996, 120(2):236-241. 10.1093/oxfordjournals.jbchem.a021404, 8889805.
61. Norambuena L, Marchant L, Berninsone P, Hirschberg CB, Silva H, Orellana A. Transport of UDP-galactose in plants. Identification and functional characterization of AtUTr1, an Arabidopsis thaliana UDP-galactos/UDP-glucose transporter. J Biol Chem 2002, 277(36):32923-32929. 10.1074/jbc.M204081200, 12042319.
62. Lytton J. Na+/Ca2+ exchangers: three mammalian gene families control Ca2+ transport. Biochem J 2007, 406(3):365-382.
63. Abraham MR, Jahangir A, Alekseev AE, Terzic A. Channelopathies of inwardly rectifying potassium channels. FASEB J 1999, 13(14):1901-1910.
64. Diener AC, Gaxiola RA, Fink GR. Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell 2001, 13(7):1625-1637. 139545, 11449055.
65. Dagan T, Artzy-Randrup Y, Martin W. Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc Natl Acad Sci U S A 2008, 105(29):10039-10044. 10.1073/pnas.0800679105, 2474566, 18632554.
66. Lapierre P, Gogarten JP. Estimating the size of the bacterial pan-genome. Trends Genet 2009, 25(3):107-110. 10.1016/j.tig.2008.12.004, 19168257.
67. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome" Proc Natl Acad Sci USA 2005, 102(39):13950-13955. 10.1073/pnas.0506758102, 1216834, 16172379.
68. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 2008, 456(7219):239-244. 10.1038/nature07410, 18923393.
69. 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(11):R88. 10.1186/gb-2004-5-11-r88, 545779, 15535864.
70. Doolittle WF, Boucher Y, Nesbo CL, Douady CJ, Andersson JO, Roger AJ. How big is the iceberg of which organellar genes in nuclear genomes are but the tip?. Philos Transac Royal Soc Lond Series B Biol Sci 2003, 358(1429):39-57. discussion 57-38.
71. O'Brien EA, Koski LB, Zhang Y, Yang L, Wang E, Gray MW, Burger G, Lang BF. TBestDB: a taxonomically broad database of expressed sequence tags (ESTs). Nucleic Acids Res 2007, 35(Database issue):D445-D451. 1899108, 17202165.
72. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Muller WE, Wetter T, Suhai S. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 2004, 14(6):1147-1159. 10.1101/gr.1917404, 419793, 15140833.
73. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797. 10.1093/nar/gkh340, 390337, 15034147.
74. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25(24):4876-4882. 10.1093/nar/25.24.4876, 147148, 9396791.
75. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McLnerney JO. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 2006, 6:29. 10.1186/1471-2148-6-29, 1435933, 16563161.
76. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704. 10.1080/10635150390235520, 14530136.
77. Felsenstein J. PHYLIP (Phylogeny Inference Package) version 3.65. Distributed by the author 2005, Seattle: Department of Genome Sciences, University of Washington.
78. Schmidt HA, Strimmer K, Vingron M, von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002, 18(3):502-504. 10.1093/bioinformatics/18.3.502, 11934758.
79. Ruiz-Trillo I, Burger G, Holland PW, King N, Lang BF, Roger AJ, Gray MW. The origins of multicellularity: a multi-taxon genome initiative. Trends Genet 2007, 23(3):113-118. 10.1016/j.tig.2007.01.005, 17275133.