Horizontally transferred genes in the genome of Pacific white shrimp, Litopenaeus vannamei

BMC Evolutionary Biology

Jian-Hai Xiang¹  Fu-Hua Li¹  Jian-Kai Wei²  Cheng-Zhang Liu¹  Xiao-Jun Zhang¹  Jian-Bo Yuan² 

[1] Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, 7, Nanhai Road, Qingdao 266071, China;University of Chinese Academy of Sciences, Beijing 100049, China

关键词: Fungi;    Bacteria;    Shrimp;    Litopenaeus vannamei;    Horizontal gene transfer;   

Others  :  1086671
DOI  :  10.1186/1471-2148-13-165

 received in 2013-02-27, accepted in 2013-08-02,  发布年份 2013

【 摘 要 】

Background

In recent years, as the development of next-generation sequencing technology, a growing number of genes have been reported as being horizontally transferred from prokaryotes to eukaryotes, most of them involving arthropods. As a member of the phylum Arthropoda, the Pacific white shrimp Litopenaeus vannamei has to adapt to the complex water environments with various symbiotic or parasitic microorganisms, which provide a platform for horizontal gene transfer (HGT).

Results

In this study, we analyzed the genome-wide HGT events in L. vannamei. Through homology search and phylogenetic analysis, followed by experimental PCR confirmation, 14 genes with HGT event were identified: 12 of them were transferred from bacteria and two from fungi. Structure analysis of these genes showed that the introns of the two fungi-originated genes were substituted by shrimp DNA fragment, two genes transferred from bacteria had shrimp specific introns inserted in them. Furthermore, around other three bacteria-originated genes, there were three large DNA segments inserted into the shrimp genome. One segment was a transposon that fully transferred, and the other two segments contained only coding regions of bacteria. Functional prediction of these 14 genes showed that 6 of them might be related to energy metabolism, and 4 others related to defense of the organism.

Conclusions

HGT events from bacteria or fungi were happened in the genome of L. vannamei, and these horizontally transferred genes can be transcribed in shrimp. This is the first time to report the existence of horizontally transferred genes in shrimp. Importantly, most of these genes are exposed to a negative selection pressure and appeared to be functional.

【 授权许可】

   
2013 Yuan et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Dunning Hotopp JC: Horizontal gene transfer between bacteria and animals. Trends Genet 2011, 27(4):157-163.
• [2]Keeling PJ, Palmer JD: Horizontal gene transfer in eukaryotic evolution. Nature reviews Genetics 2008, 9(8):605-618.
• [3]Beiko RG, Harlow TJ, Ragan MA: Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA 2005, 102(40):14332-14337.
• [4]Gogarten JP, Doolittle WF, Lawrence JG: Prokaryotic evolution in light of gene transfer. Mol Biol Evol 2002, 19(12):2226-2238.
• [5]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 research 2008, 18(2):272-280.
• [6]McNulty SN, Foster JM, Mitreva M, Dunning Hotopp JC, Martin J, Fischer K, Wu B, Davis PJ, Kumar S, Brattig NW, et al.: Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PloS one 2010, 5(6):e11029.
• [7]Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, et al.: The dynamic genome of Hydra. Nature 2010, 464(7288):592-596.
• [8]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
• [9]Chan CX, Bhattacharya D, Reyes-Prieto A: Endosymbiotic and horizontal gene transfer in microbial eukaryotes: impacts on cell evolution and the tree of life. Mobile genetic elements 2012, 2(2):101-105.
• [10]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. Nature genetics 2006, 38(8):953-956.
• [11]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 U S A 2008, 105(46):17867-17871.
• [12]Moran NA, Jarvik T: Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 2010, 328(5978):624-627.
• [13]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 genetics 2010, 6(2):e1000827.
• [14]Lightner DV: A review of the diseases of cultured penaeid shrimps and prawns with emphasis on recent discoveries and developments. Iloilo City, Philippines: Proceedings of the First International Conference on the Culture of Penaeid Prawns/Shrimps, 4–7 December 1984; 1985:79-103.
• [15]Klaoudatos SD, Klaoudatos DS: Phylogeny biology and ecology of Crustaceans(Phylum Arthropoda; Subphylum Crusacea). Reproductive Biology of Crustaceans. New Hampshire, USA: Case studies of Decapod Crustaceans Science Publishers; 2008.
• [16]Center GSL: The brine shrimp life cycle. Genetics: Learn; 2012.
• [17]Gil-Turnes MS, Hay ME, Fenical W: Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 1989, 246(4926):116-118.
• [18]Overstreet RM: Parasites of some penaeid shrimps with emphasis on reared hosts. Aquaculture 1973, 2:105-140.
• [19]DiGuistini S, Wang Y, Liao NY, Taylor G, Tanguay P, Feau N, Henrissat B, Chan SK, Hesse-Orce U, Alamouti SM, et al.: Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proc Natl Acad Sci USA 2011, 108(6):2504-2509.
• [20]O’Leary NA, Trent HF 3rd, Robalino J, Peck ME, McKillen DJ, Gross PS: Analysis of multiple tissue-specific cDNA libraries from the Pacific whiteleg shrimp, Litopenaeus vannamei. Integrative and comparative biology 2006, 46(6):931-939.
• [21]Li C, Weng S, Chen Y, Yu X, Lu L, Zhang H, He J, Xu X: Analysis of Litopenaeus vannamei transcriptome using the next-generation DNA sequencing technique. PloS one 2012, 7(10):e47442.
• [22]Li ZW, Shen YH, Xiang ZH, Zhang Z: Pathogen-origin horizontally transferred genes contribute to the evolution of Lepidopteran insects. BMC evolutionary biology 2011, 11:356. BioMed Central Full Text
• [23]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.
• [24]Sutton BC: Mitosporic fungi (Deuteromycetes) in the fictionary-of-the-fungi. 1993, 27-55. [Fungal Holomorph : Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics] http://apps.webofknowledge.com/InboundService.do?SID=T2mU3W69zf7xznsDuJS&product=WOS&UT=A1993BY77H00003&SrcApp=EndNote&DestFail=http%3A%2F%2Fwww.webofknowledge.com&Init=Yes&action=retrieve&Func=Frame&customersID=ResearchSoft&SrcAuth=ResearchSoft&IsProductCode=Yes&mode=FullRecord webcite
• [25]Altincicek B, Kovacs JL, Gerardo NM: Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol Lett 2012, 8(2):253-257.
• [26]Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA: Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 1997, 387(6632):489-493.
• [27]Iyer LM, Aravind L, Coon SL, Klein DC, Koonin EV: Evolution of cell-cell signaling in animals: did late horizontal gene transfer from bacteria have a role? Trends in genetics : TIG 2004, 20(7):292-299.
• [28]Li DX, Du XJ, Zhao XF, Wang JX: Cloning and expression analysis of an o-methyltransferase (OMT) gene from Chinese shrimp, Fenneropenaeus chinensis. Fish & shellfish immunol 2006, 21(3):284-292.
• [29]Li R, Li Y, Fang X, Yang H, Wang J, Kristiansen K: SNP detection for massively parallel whole-genome resequencing. Genome research 2009, 19(6):1124-1132.
• [30]Gilbert C, Schaack S, Pace JK 2nd, Brindley PJ, Feschotte C: A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 2010, 464(7293):1347-1350.
• [31]Rodelsperger C, Sommer RJ: Computational archaeology of the Pristionchus pacificus genome reveals evidence of horizontal gene transfers from insects. BMC evolutionary biology 2011, 11:239. BioMed Central Full Text
• [32]Moeck GS, Coulton JW: TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol Microbiol 1998, 28(4):675-681.
• [33]Stanke M, Morgenstern B: AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 2005, 33:W465-W467.
• [34]Majoros WH, Pertea M, Salzberg SL: TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 2004, 20(16):2878-2879.
• [35]Burge C, Karlin S: Prediction of complete gene structures in human genomic DNA. J Mol Biol 1997, 268(1):78-94.
• [36]Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J: KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics, proteomics & bioinformatics 2006, 4(4):259-263.
• [37]Nikoh N, Nakabachi A: Aphids acquired symbiotic genes via lateral gene transfer. BMC biology 2009, 7:12. BioMed Central Full Text
• [38]Peters AE, Bavishi A, Cho H, Choudhary M: Evolutionary constraints and expression analysis of gene duplications in Rhodobacter sphaeroides 2.4.1. BMC research notes 2012, 5:192. BioMed Central Full Text
• [39]Kornberg HL: Krebs citric-acid cycle - half a century and still turning - introductory. Biochem Soc Symp 1987, 54:1-2.
• [40]Karp G: Cell and Molecular Biology. John Wiley & Sons; 2012. http://as.wiley.com/WileyCDA/WileyTitle/productCd-EHEP002533.html webcite
• [41]Schwer B, Bunkenborg J, Verdin RO, Andersen JS, Verdin E: Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc Natl Acad Sci USA 2006, 103(27):10224-10229.
• [42]Schnell JR, Dyson HJ, Wright PE: Structure, dynamics, and catalytic function of dihydrofolate reductase. Annu Rev Bioph Biom 2004, 33:119-140.
• [43]Giordani R, Buc J: Evidence for two different electron transfer pathways in the same enzyme, nitrate reductase A from Escherichia coli. Eur J Biochem/FEBS 2004, 271(12):2400-2407.
• [44]Li XZ, Luo QW, Wofford NQ, Keller KL, McInerney MJ, Wall JD, Krumholz LR: A molybdopterin oxidoreductase is involved in H-2 oxidation in desulfovibrio desulfuricans G20. J Bacteriol 2009, 191(8):2675-2682.
• [45]Higgs PI, Larsen RA, Postle K: Quantification of known components of the Escherichia coli TonB energy transduction system: TonB, ExbB, ExbD and FepA. Mol Microbiol 2002, 44(1):271-281.
• [46]Eick-Helmerich K, Braun V: Import of biopolymers into Escherichia coli: nucleotide sequences of the exbB and exbD genes are homologous to those of the tolQ and tolR genes, respectively. J Bacteriol 1989, 171(9):5117-5126.
• [47]Letain TE, Postle K: TonB protein appears to transduce energy by shuttling between the cytoplasmic membrane and the outer membrane in Escherichia coli. Mol Microbiol 1997, 24(2):271-283.
• [48]Tsuji J, Frith MC, Tomii K, Horton P: Mammalian NUMT insertion is non-random. Nucleic acids research 2012, 40(18):9073-9088.
• [49]Bork P: Hundreds of ankyrin-like repeats in functionally diverse proteins - mobile modules that cross phyla horizontally. Proteins 1993, 17(4):363-374.
• [50]Shaw WV, Packman LC, Burleigh BD, Dell A, Morris HR, Hartley BS: Primary structure of a chloramphenicol acetyltransferase specified by R plasmids. Nature 1979, 282(5741):870-872.
• [51]Harwood JH, Smith DH: Resistance factor-mediated streptomycin resistance. J Bacteriol 1969, 97(3):1262-1271.
• [52]Hahlbrock K, Scheel D: Physiology and molecular-biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 1989, 40:347-369.
• [53]Chiron H, Drouet A, Claudot AC, Eckerskorn C, Trost M, Heller W, Ernst D, Sandermann H: Molecular cloning and functional expression of a stress-induced multifunctional O-methyltransferase with pinosylvin methyltransferase activity from Scots pine (Pinus sylvestris L.). Plant Mol Biol 2000, 44(6):733-745.
• [54]Beaber JW, Hochhut B, Waldor MK: SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 2004, 427(6969):72-74.
• [55]Little JW, Mount DW, Yanischperron CR: Purified lexa protein is a repressor of the reca and lexa genes. Proc Natl Acad Sci U S A 1981, 78(7):4199-4203.
• [56]Jeffares DC, Mourier T, Penny D: The biology of intron gain and loss. Trends in genetics: TIG 2006, 22(1):16-22.
• [57]Eyre-Walker A, Keightley PD: The distribution of fitness effects of new mutations. Nat Rev Genet 2007, 8(8):610-618.
• [58]Dyall SD, Brown MT, Johnson PJ: Ancient invasions: from endosymbionts to organelles. Science 2004, 304(5668):253-257.
• [59]Kondo N, Nikoh N, Ijichi N, Shimada M, Fukatsu T: Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci USA 2002, 99(22):14280-14285.
• [60]Aikawa T, Anbutsu H, Nikoh N, Kikuchi T, Shibata F, Fukatsu T: Longicorn beetle that vectors pinewood nematode carries many Wolbachia genes on an autosome. P R Soc B 2009, 276(1674):3791-3798.
• [61]Doudoumis V, Alam U, Aksoy E, Abd-Alla AMM, Tsiamis G, Brelsfoard C, Aksoy S, Bourtzis K: Tsetse-Wolbachia symbiosis: comes of age and has great potential for pest and disease control. J Invertebr Pathol 2013, 112:S94-S103.
• [62]Hotopp JCD, Clark ME, Oliveira DCSG, Foster JM, Fischer P, Torres MC, Giebel JD, Kumar N, Ishmael N, Wang SL, et al.: Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317(5845):1753-1756.
• [63]Richards TA, Soanes DM, Jones MD, Vasieva O, Leonard G, Paszkiewicz K, Foster PG, Hall N, Talbot NJ: Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci USA 2011, 108(37):15258-15263.
• [64]Wolf YI, Rogozin IB, Kondrashov AS, Koonin EV: Genome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context. Genome research 2001, 11(3):356-372.
• [65]Dam P, Olman V, Harris K, Su ZC, Xu Y: Operon prediction using both genome-specific and general genomic information. Nucleic acids research 2007, 35(1):288-298.
• [66]Allen GC, Kornberg A: Assembly of the Primosome of DNA-Replication in Escherichia-Coli. J Biol Chem 1993, 268(26):19204-19209.
• [67]Masai H, Arai K: Operon structure of dnaT and dnaC genes essential for normal and stable DNA replication of Escherichia coli chromosome. J Biol Chem 1988, 263(29):15083-15093.
• [68]Zimmermann K, Engeser M, Blunt JW, Munro MH, Piel J: Pederin-type pathways of uncultivated bacterial symbionts: analysis of o-methyltransferases and generation of a biosynthetic hybrid. J Am Chem Soc 2009, 131(8):2780-2781.
• [69]Sanchez-Paz A, Garcia-Carreno F, Hernandez-Lopez J, Muhlia-Almazan A, Yepiz-Plascencia G: Effect of short-term starvation on hepatopancreas and plasma energy reserves of the Pacific white shrimp (Litopenaeus vannamei). J Exp Mar Biol Ecol 2007, 340(2):184-193.
• [70]Robalino J, Almeida JS, McKillen D, Colglazier J, Trent HF 3rd, Chen YA, Peck ME, Browdy CL, Chapman RW, Warr GW, et al.: Insights into the immune transcriptome of the shrimp Litopenaeus vannamei: tissue-specific expression profiles and transcriptomic responses to immune challenge. Physiological genomics 2007, 29(1):44-56.
• [71]Huang X, Madan A: CAP3: A DNA sequence assembly program. Genome research 1999, 9(9):868-877.
• [72]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 research 1997, 25(17):3389-3402.
• [73]Higgins DG, Thompson JD, Gibson TJ: Using CLUSTAL for multiple sequence alignments. Methods in enzymology 1996, 266:383-402.
• [74]Ropelewski AJ, Nicholas HB, Gonzalez Mendez RR: MPI-PHYLIP: parallelizing computationally intensive phylogenetic analysis routines for the analysis of large protein families. PloS one 2010, 5(11):e13999.
• [75]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
• [76]Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular biology and evolution 2000, 17(4):540-552.
• [77]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic biology 2003, 52(5):696-704.
• [78]Anisimova M, Gascuel O: Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Systematic biology 2006, 55(4):539-552.
• [79]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574.
• [80]Li Q, Liu QH, Huang J: FATP synthase b-chain of Litopenaeus vannamei involved in White Spot Syndrome Virus infection. Virus genes 2013. http://dx.doi.org/10.1007/s11262-013-0907-1 webcite. http://link.springer.com/article/10.1007%2Fs11262-013-0907-1 webcite
• [81]Li S, Zhang X, Sun Z, Li F, Xiang J: Transcriptome analysis on Chinese shrimp fenneropenaeus chinensis during WSSV acute infection. PloS one 2013, 8(3):e58627.
• [82]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, et al.: Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29(7):644-U130.
• [83]Robinson MD, McCarthy DJ, Smyth GK: edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26(1):139-140.
• [84]Bullard JH, Purdom E, Hansen KD, Dudoit S: Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC bioinformatics 2010, 11:94. BioMed Central Full Text
• [85]Twine NA, Janitz K, Wilkins MR, Janitz M: Whole transcriptome sequencing reveals gene expression and splicing differences in brain regions affected by Alzheimer’s disease. PloS one 2011, 6(1):e16266.
• [86]Benjamini Y, Hochberg Y: Controlling the false discovery rate - apractical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995, 57(1):289-300.
• [87]Winbush A, Reed D, Chang PL, Nuzhdin SV, Lyons LC, Arbeitman MN: Identification of gene expression changes associated with long-term memory of courtship rejection in Drosophila males. G3 (Bethesda) 2012, 2(11):1437-1445.