Detection and Characterization of Wolbachia Infections in Natural Populations of Aphids: Is the Hidden Diversity Fully Unraveled?

PLoS ONE - Tập 6 Số 12 - Trang e28695
A. A. Augustinos1,2, Diego Santos-García3, Eva Dionyssopoulou1,2, Marta Moreira4, Aristeidis P. Papapanagiotou5, Marios Scarvelakis1, Vangelis Doudoumis1,2, Silvia Ramos3, A. M. Franquinho Aguiar6, Paulo A. V. Borges7, Manhaz Khadem4, Amparo Latorre3,8, George Tsiamis1,2, Kostas Bourtzis9,1,2
1Department of Environmental and Natural Resources Management, University of Ioannina, Agrinio, Greece
2Department of Environmental and Natural Resources Management, University of Western Greece, Agrinio, Greece
3Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, Valencia, Spain
4ISOPlexis Gene Bank, Universidade da Madeira, Funchal, Portugal
5Department of Greenhouse Crops and Floriculture, Technological Educational Institute of Messolonghi, Messolonghi, Greece
6Laboratório de Qualidade Agrícola, Núcleo de Fitopatologia,, Madeira, Portugal
7Departamento de Ciências Agrárias CITA-A (Azorean Biodiversity Group), Universidade dos Açores, Angra do Heroísmo, Terceira – Azores
8Área de Genómica y Salud, Centro Superior de Investigación en Salud Pública (CSISP), Valencia, Spain
9Biomedical Sciences Research Center Al. Fleming, Vari, Greece

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JH Werren, 1997, Biology of <italic>Wolbachia</italic>., Annu Rev Entomol, 42, 587, 10.1146/annurev.ento.42.1.587

FM Aguiar, 2001, Aphids (Homoptera: Aphidoidea) from Madeira Island – New records and corrections., Boletin sanidade Vegetal, Plagas, 27, 323

A Saridaki, 2010, <italic>Wolbachia</italic>: more than just a bug in insects genitals., Curr Opin Microbiol, 13, 67, 10.1016/j.mib.2009.11.005

C Bandi, 1998, Phylogeny of <italic>Wolbachia</italic> in filarial nematodes., Proc Biol Sci, 265, 2407, 10.1098/rspb.1998.0591

JH Werren, 2000, <italic>Wolbachia</italic> infection frequencies in insects: evidence of a global equilibrium?, Proc Biol Sci, 267, 1277, 10.1098/rspb.2000.1139

A Jeyaprakash, 2000, Long PCR improves <italic>Wolbachia</italic> DNA amplification: wsp sequences found in 76% of sixty-three arthropod species., Insect Mol Biol, 9, 393, 10.1046/j.1365-2583.2000.00203.x

K Hilgenboecker, 2008, How many species are infected with <italic>Wolbachia</italic>? statistical analysis of current data., FEMS Microbiol Lett, 281, 215, 10.1111/j.1574-6968.2008.01110.x

E Ferri, 2011, New insights into the evolution of <italic>Wolbachia</italic> infections in filarial nematodes inferred from a large range of screened species., PLoS One, 6, e20843, 10.1371/journal.pone.0020843

N Lo, 2007, Taxonomic status of the intracellular bacterium <italic>Wolbachia pipientis</italic>., Int J Syst Evol Microbiol, 57, 654, 10.1099/ijs.0.64515-0

JH Werren, 1995, Evolution and phylogeny of <italic>Wolbachia</italic>: reproductive parasites of arthropods., Proc Biol Sci, 261, 55, 10.1098/rspb.1995.0117

TT Vandekerckhove, 1999, Phylogenetic analysis of the 16S rDNA of the cytoplasmic bacterium <italic>Wolbachia</italic> from the novel host Folsomia candida (Hexapoda, Collembola) and its implications for wolbachial taxonomy., FEMS Microbiol Lett, 180, 279, 10.1111/j.1574-6968.1999.tb08807.x

N Lo, 2002, How many <italic>wolbachia</italic> supergroups exist?, Mol Biol Evol, 19, 341, 10.1093/oxfordjournals.molbev.a004087

PA Vaishampayan, 2007, Molecular evidence and phylogenetic affiliations of <italic>Wolbachia</italic> in cockroaches., Mol Phylogenet Evol, 44, 1346, 10.1016/j.ympev.2007.01.003

AK Dunn, 2005, Culture-independent characterization of the microbiota of the ant lion <italic>Myrmeleon mobilis</italic> (Neuroptera: Myrmeleontidae)., Appl Environ Microbiol, 71, 8784, 10.1128/AEM.71.12.8784-8794.2005

S Bordenstein, 2005, Discovery of a novel <italic>Wolbachia</italic> super group in Isoptera., Curr Microbiol, 51, 393, 10.1007/s00284-005-0084-0

A Haegeman, 2009, An endosymbiotic bacterium in a plant-parasitic nematode: member of a new <italic>Wolbachia</italic> supergroup., Int J Parasitol, 39, 1045, 10.1016/j.ijpara.2009.01.006

VI Ros, 2009, How diverse is the genus <italic>Wolbachia</italic>? Multiple-gene sequencing reveals a putatively new <italic>Wolbachia</italic>supergroup recovered from spider mites (Acari: Tetranychidae)., Appl Environ Microbiol, 75, 1036, 10.1128/AEM.01109-08

SM Rowley, 2004, <italic>Wolbachia pipientis</italic> in Australian spiders., Curr Microbiol, 49, 208, 10.1007/s00284-004-4346-z

L Baldo, 2007, <italic>Wolbachia</italic> are present in southern african scorpions and cluster with supergroup F., Curr Microbiol, 55, 367, 10.1007/s00284-007-9009-4

L Baldo, 2006, Multilocus sequence typing system for the endosymbiont <italic>Wolbachia pipientis</italic>., Appl Environ Microbiol, 72, 7098, 10.1128/AEM.00731-06

C Paraskevopoulos, 2006, Toward a <italic>Wolbachia</italic> multilocus sequence typing system: discrimination of <italic>Wolbachia</italic> strains present in Drosophila species., Curr Microbiol, 53, 388, 10.1007/s00284-006-0054-1

R Stouthamer, 1999, <italic>Wolbachia pipientis</italic>: microbial manipulator of arthropod reproduction., Annu Rev Microbiol, 53, 71, 10.1146/annurev.micro.53.1.71

PA Hancock, 2011, Population dynamic models of the spread of <italic>Wolbachia</italic>., Am Nat, 177, 323, 10.1086/658121

K Bourtzis, 1998, Rescuing <italic>Wolbachia</italic> have been overlooked., Nature, 391, 852, 10.1038/36017

K Bourtzis, 2006, Insect pest control using <italic>Wolbachia</italic> and/or radiation., 225

K Bourtzis, 2008, <italic>Wolbachia</italic>-based technologies for insect pest population control., Adv Exp Med Biol, 627, 104, 10.1007/978-0-387-78225-6_9

H Laven, 1967, Eradication of <italic>Culex pipiens fatigans</italic> through cytoplasmic incompatibility., Nature, 216, 383, 10.1038/216383a0

S Zabalou, 2004, <italic>Wolbachia</italic>-induced cytoplasmic incompatibility as a means for insect pest population control., Proc Natl Acad Sci U S A, 101, 15042, 10.1073/pnas.0403853101

Z Xi, 2005, Generation of a novel <italic>Wolbachia</italic> infection in <italic>Aedes albopictus</italic> (Asian tiger mosquito) via embryonic microinjection., Insect Biochem Mol Biol, 35, 903, 10.1016/j.ibmb.2005.03.015

Z Kambris, 2009, Immune activation by life-shortening <italic>Wolbachia</italic> and reduced filarial competence in mosquitoes., Science, 326, 134, 10.1126/science.1177531

AP Turley, 2009, <italic>Wolbachia</italic> infection reduces blood-feeding success in the dengue fever mosquito, <italic>Aedes aegypti</italic>., PLoS Negl Trop Dis, 3, e516, 10.1371/journal.pntd.0000516

S Zabalou, 2009, Incompatible insect technique: incompatible males from a <italic>Ceratitis capitata</italic> genetic sexing strain., Entomologia Experimentalis et Applicata, 132, 232, 10.1111/j.1570-7458.2009.00886.x

A Apostolaki, 2011, Transinfection of the olive fruit fly <italic>Bactrocera oleae</italic> with <italic>Wolbachia</italic>: towards a symbiont-based population control strategy., Journal of Applied Entomology, 135, 546, 10.1111/j.1439-0418.2011.01614.x

CJ McMeniman, 2009, Stable introduction of a life-shortening <italic>Wolbachia</italic> infection into the mosquito <italic>Aedes aegypti</italic>., Science, 323, 141, 10.1126/science.1165326

LA Moreira, 2009, A <italic>Wolbachia</italic> symbiont in <italic>Aedes aegypti</italic> limits infection with dengue, Chikungunya and Plasmodium., Cell, 139, 1268, 10.1016/j.cell.2009.11.042

LM Hedges, 2008, <italic>Wolbachia</italic> and virus protection in insects., Science, 322, 702, 10.1126/science.1162418

L Teixeira, 2008, The bacterial symbiont <italic>Wolbachia</italic> induces resistance to RNA viral infections in <italic>Drosophila melanogaster</italic>., PLoS Biol, 6, e2, 10.1371/journal.pbio.1000002

G Bian, 2010, The endosymbiotic bacterium <italic>Wolbachia</italic> induces resistance to dengue virus in <italic>Aedes aegypti</italic>., PLoS Pathog, 6, e1000833, 10.1371/journal.ppat.1000833

PE Cook, 2010, <italic>Wolbachia pipientis</italic>: an expanding bag of tricks to explore for disease control., Trends Parasitol, 26, 373, 10.1016/j.pt.2010.05.006

RL Glaser, 2010, The native <italic>Wolbachia</italic> endosymbionts of <italic>Drosophila melanogaster</italic> and <italic>Culex quinquefasciatus</italic> increase host resistance to West Nile virus infection., PLoS One, 5, e11977, 10.1371/journal.pone.0011977

AFG Dixon, 1987, Why There are So Few Species of Aphids, Especially in the Tropics., The American Naturalist, 129, 580, 10.1086/284659

M Schadler, 2007, Antagonistic interactions between plant competition and insect herbivory., Ecology, 88, 1490, 10.1890/06-0647

V Brault, 2010, Transcriptomic analysis of intestinal genes following acquisition of pea enation mosaic virus by the pea aphid <italic>Acyrthosiphon pisum</italic>., J Gen Virol, 91, 802, 10.1099/vir.0.012856-0

AE Douglas, 2006, Phloem-sap feeding by animals: Problems and solutions., Journal of Experimental Botany, 57, 747, 10.1093/jxb/erj067

KM Oliver, 2010, Facultative Symbionts in Aphids and the Horizontal Transfer of Ecologically Important Traits., Annual Review of Entomology, 55, 247, 10.1146/annurev-ento-112408-085305

AE Douglas, 1997, Parallels and contrasts between symbiotic bacteria and bacterial-derived organelles: evidence from <italic>Buchnera</italic>, the bacterial symbiont of aphids., FEMS MicrobiologyEcology, 24, 1, 10.1111/j.1574-6941.1997.tb00418.x

P Baumann, 2005, Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects., Annu Rev Microbiol, 59, 155, 10.1146/annurev.micro.59.030804.121041

A Moya, 2008, Learning how to live together: genomic insights into prokaryote-animal symbioses., Nat Rev Genet, 9, 218, 10.1038/nrg2319

L Brinza, 2009, Systemic analysis of the symbiotic function of <italic>Buchnera aphidicola</italic>, the primary endosymbiont of the pea aphid <italic>Acyrthosiphon pisum</italic>., C R Biol, 332, 1034, 10.1016/j.crvi.2009.09.007

KM Oliver, 2005, Variation in resistance to parasitism in aphids is due to symbionts not host genotype., Proc Natl Acad Sci U S A, 102, 12795, 10.1073/pnas.0506131102

C Vorburger, 2010, A strain of the bacterial symbiont <italic>Regiella insecticola</italic> protects aphids against parasitoids., Biol Lett, 6, 109, 10.1098/rsbl.2009.0642

CB Montllor, 2002, Facultative bacterial endosymbionts benefit pea aphids <italic>Acyrthosiphon pisum</italic> under heat stress., Ecological Entomology, 27, 189, 10.1046/j.1365-2311.2002.00393.x

NA Moran, 2010, Lateral transfer of genes from fungi underlies carotenoid production in aphids., Science, 328, 624, 10.1126/science.1187113

N Nikoh, 2010, Bacterial genes in the aphid genome: absence of functional gene transfer from <italic>Buchnera</italic> to its host., PLoS Genet, 6, e1000827, 10.1371/journal.pgen.1000827

V Perez-Brocal, 2006, A small microbial genome: the end of a long symbiotic relationship?, Science, 314, 312, 10.1126/science.1130441

MJ Gosalbes, 2008, The striking case of tryptophan provision in the cedar aphid <italic>Cinara cedri</italic>., J Bacteriol, 190, 6026, 10.1128/JB.00525-08

SA West, 1998, <italic>Wolbachia</italic> in two insect host-parasitoid communities., Mol Ecol, 7, 1457, 10.1046/j.1365-294x.1998.00467.x

T Tsuchida, 2002, Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, <italic>Acyrthosiphon pisum</italic>., Mol Ecol, 11, 2123, 10.1046/j.1365-294X.2002.01606.x

A Nirgianaki, 2003, <italic>Wolbachia</italic> infections of the whitefly <italic>Bemisia tabaci</italic>., Curr Microbiol, 47, 93, 10.1007/s00284-002-3969-1

L Gomez-Valero, 2004, Coexistence of <italic>Wolbachia</italic> with <italic>Buchnera aphidicola</italic> and a secondary symbiont in the aphid <italic>Cinara cedri</italic>., J Bacteriol, 186, 6626, 10.1128/JB.186.19.6626-6633.2004

Z Wang, 2009, Distribution and diversity of <italic>Wolbachia</italic> in different populations of the wheat aphid <italic>Sitobion miscanthi</italic> (Hemiptera: Aphididae) in China., European Journal of Entomology, 106, 49, 10.14411/eje.2009.007

B Ortiz-Rivas, 2010, Combination of molecular data support the existence of three main lineages in the phylogeny of aphids (Hemiptera: Aphididae) and the basal position of the subfamily Lachninae., Mol Phylogenet Evol, 55, 305, 10.1016/j.ympev.2009.12.005

W Zhou, 1998, Phylogeny and PCR-based classification of <italic>Wolbachia</italic> strains using <italic>wsp</italic> gene sequences., Proc Biol Sci, 265, 509, 10.1098/rspb.1998.0324

M Casiraghi, 2005, Phylogeny of <italic>Wolbachia pipientis</italic> based on <italic>gltA</italic>, <italic>groEL</italic> and <italic>ftsZ</italic> gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the <italic>Wolbachia</italic> tree., Microbiology, 151, 4015, 10.1099/mic.0.28313-0

JA Breeuwer, 1992, Phylogeny of cytoplasmic incompatibility micro-organisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences., Insect Mol Biol, 1, 25, 10.1111/j.1365-2583.1993.tb00074.x

R Stouthamer, 1993, Molecular identification of microorganisms associated with parthenogenesis., Nature, 361, 66, 10.1038/361066a0

GR Burke, 2009, Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae., Appl Environ Microbiol, 75, 5328, 10.1128/AEM.00717-09

A Lamelas, 2011, New Clues about the Evolutionary History of Metabolic Losses in Bacterial Endosymbionts, Provided by the Genome of <italic>Buchnera aphidicola</italic> from the Aphid <italic>Cinara tujafilina</italic>., Appl Environ Microbiol, 77, 4446, 10.1128/AEM.00141-11

SP Sinkins, 1995, <italic>Wolbachia</italic> superinfections and the expression of cytoplasmic incompatibility., Proc Biol Sci, 261, 325, 10.1098/rspb.1995.0154

SL Dobson, 2002, Characterization of <italic>Wolbachia</italic> host cell range via the in vitro establishment of infections., Appl Environ Microbiol, 68, 656, 10.1128/AEM.68.2.656-660.2002

M Reuter, 2003, High levels of multiple <italic>Wolbachia</italic> infection and recombination in the ant <italic>Formica exsecta</italic>., Mol Biol Evol, 20, 748, 10.1093/molbev/msg082

Y Kikuchi, 2003, Diversity of <italic>Wolbachia</italic> endosymbionts in heteropteran bugs., Appl Environ Microbiol, 69, 6082, 10.1128/AEM.69.10.6082-6090.2003

O Duron, 2005, Transposable element polymorphism of <italic>Wolbachia</italic> in the mosquito <italic>Culex pipiens</italic>: evidence of genetic diversity, superinfection and recombination., Mol Ecol, 14, 1561, 10.1111/j.1365-294X.2005.02495.x

ZX Li, 2005, Molecular differentiation of the B biotype from other biotypes of <italic>Bemisia tabaci</italic> (Hemiptera: Aleyrodidae), based on internally transcribed spacer 1 sequences., European Journal of Entomology, 102, 293, 10.14411/eje.2005.041

ZX Li, 2007, Prevalence of <italic>Wolbachia</italic> infection in <italic>Bemisia tabaci</italic>., Curr Microbiol, 54, 467, 10.1007/s00284-007-0011-7

SL O'Neill, 1992, 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects., Proc Natl Acad Sci U S A, 89, 2699, 10.1073/pnas.89.7.2699

PM Simoes, 2011, Wolbachia detection: an assessment of standard PCR protocols., Mol Ecol Resour, 11, 567, 10.1111/j.1755-0998.2010.02955.x

W Arthofer, 2009, Hidden <italic>Wolbachia</italic> diversity in field populations of the European cherry fruit fly, <italic>Rhagoletis cerasi</italic> (Diptera, Tephritidae)., Mol Ecol, 18, 3816, 10.1111/j.1365-294X.2009.04321.x

WJ Miller, 2010, Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behaviour of <italic>Drosophila paulistorum</italic>., PLoS Pathog, e1001214, 10.1371/journal.ppat.1001214

W Arthofer, 2011, Allele intersection analysis: a novel tool for multi locus sequence assignment in multiply infected hosts., PLoS One, 6, e22198, 10.1371/journal.pone.0022198

L Mouton, 2003, Strain-specific regulation of intracellular <italic>Wolbachia</italic> density in multiply infected insects., Mol Ecol, 12, 3459, 10.1046/j.1365-294X.2003.02015.x

N Kondo, 2005, Infection density of <italic>Wolbachia</italic> endosymbiont affected by co-infection and host genotype., Biol Lett, 1, 488, 10.1098/rsbl.2005.0340

E Vautrin, 2009, Interactions between vertically transmitted symbionts: cooperation or conflict?, Trends Microbiol, 17, 95, 10.1016/j.tim.2008.12.002

N Kondo, 2002, Genome fragment of <italic>Wolbachia</italic> endosymbiont transferred to X chromosome of host insect., Proc Natl Acad Sci U S A, 99, 14280, 10.1073/pnas.222228199

K Fenn, 2006, Phylogenetic relationships of the <italic>Wolbachia</italic> of nematodes and arthropods., PLoS Pathog, 2, e94, 10.1371/journal.ppat.0020094

JC Dunning Hotopp, 2007, Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes., Science, 317, 1753, 10.1126/science.1142490

SN McNulty, 2010, Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer., PLoS One, 5, e11029, 10.1371/journal.pone.0011029

V Doudoumis, 2011, Detection and characterization of <italic>Wolbachia</italic> infections in laboratory and natural populations of different species of tse-tse flies (genus <italic>Glossina</italic>)., BMC Microbiology

2010, Genome sequence of the pea aphid <italic>Acyrthosiphon pisum</italic>., PLoS Biol, 8, e1000313, 10.1371/journal.pbio.1000313

P Buchner, 1965, Endosymbiosis of Animals with Plant Microorganisms

NA Moran, 2005, The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes., Proc Natl Acad Sci U S A, 102, 16919, 10.1073/pnas.0507029102

PH Degnan, 2009, <italic>Hamiltonella defensa</italic>, genome evolution of protective bacterial endosymbiont from pathogenic ancestors., Proc Natl Acad Sci U S A, 106, 9063, 10.1073/pnas.0900194106

PH Degnan, 2009, Dynamics of genome evolution in facultative symbionts of aphids., Environ Microbiol, 12, 2060, 10.1111/j.1462-2920.2009.02085.x

GR Burke, 2009, Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae., Appl Environ Microbiol, 75, 5328, 10.1128/AEM.00717-09

A Lamelas, 2011, New Clues about the Evolutionary History of Metabolic Losses in Bacterial Endosymbionts, Provided by the Genome of <italic>Buchnera aphidicola</italic> from the Aphid <italic>Cinara tujafilina</italic>., Appl Environ Microbiol, 77, 4446, 10.1128/AEM.00141-11

T Hosokawa, 2010, <italic>Wolbachia</italic> as a bacteriocyte-associated nutritional mutualist., Proc Natl Acad Sci U S A, 107, 769, 10.1073/pnas.0911476107

OE Heie, 2004, The history of the studies on aphid palaeontology and their bearing on the evolutionary history of aphids

FM Aguiar, 2001, Aphids (Homoptera: Aphidoidea) from Madeira Island – New records and corrections., Boletin sanidade Vegetal, Plagas, 27, 323

RL Blackman, 1984, Aphids on the world&apos;s crops: an identification and information guide

RL Blackman, 2000, Aphids on the world&apos;s crops: an identification and information guide

G Remaudiere, 1997, Catalogue des Aphididae du Monde.

A Latorre, 1986, Evolution of mitochondrial DNA in <italic>Drosophila subobscura</italic>., Proc Natl Acad Sci U S A, 83, 8649, 10.1073/pnas.83.22.8649

JJ Doyle, 1990, Isolation of plant DNA from fresh tissue., Focus, 12, 13

R Hanner, 1997, Branchiopod phylogenetic reconstruction from 12S rDNA sequence data., Journal of Crustacean Biology, 17, 174, 10.2307/1549471

JL Hartley, 2003, PEG precipitation for selective removal of small DNA fragments., Focus, 25, 18

DW Reed, 2002, Microbial communities from methane hydrate-bearing deep marine sediments in a forearc basin., Appl Environ Microbiol, 68, 3759, 10.1128/AEM.68.8.3759-3770.2002

RC Edgar, 2004, MUSCLE: multiple sequence alignment with high accuracy and high throughput., Nucleic Acids Res, 32, 1792, 10.1093/nar/gkh340

JD Thompson, 1994, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice., Nucleic Acids Res, 22, 4673, 10.1093/nar/22.22.4673

DL Swofford, 2000, PAUP: phylogenetic analysis using parsimony, 4.0, beta version 4a ed.

F Ronquist, 2003, MrBayes 3: Bayesian phylogenetic inference under mixed models., Bioinformatics, 19, 1572, 10.1093/bioinformatics/btg180

L Heath, 2006, Recombination patterns in aphthoviruses mirror those found in other picornaviruses., J Virol, 80, 11827, 10.1128/JVI.01100-06