BMC Microbiology | |
Diversity of culturable bacteria including Pantoea in wild mosquito Aedes albopictus | |
Patrick Mavingui3  Pierre Ravelonandro2  Fara Nantenaina Raharimalala1  Florence Hélène Tran3  Claire Valiente Moro3  | |
[1] Present address: Medical Entomology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar;Centre National de Recherche sur l′Environnement, Antananarivo, Madagascar;Ecologie Microbienne, CNRS UMR 5557, INRA USC1364, VetAgroSup,, Villeurbanne, France | |
关键词: Plasmids; Pantoea; Asian tiger mosquito; Culturable bacteria; | |
Others : 1144039 DOI : 10.1186/1471-2180-13-70 |
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received in 2012-11-30, accepted in 2013-03-20, 发布年份 2013 | |
【 摘 要 】
Background
The microbiota has been shown to play an important role in the biology of insects. In recent decades, significant efforts have been made to better understand the diversity of symbiotic bacteria associated with mosquitoes and assess their influence on pathogen transmission. Here, we report the bacterial composition found in field-caught Aedes albopictus populations by using culture-dependent methods.
Results
A total of 104 mosquito imagos (56 males and 48 females) were caught from four contrasting biotopes of Madagascar and their bacterial contents were screened by plating whole body homogenates on three different culture media. From 281 bacterial colony types obtained, amplified ribosomal DNA restriction analysis (ARDRA) showed they had 40 distinct ribotypes. Sequencing and BLAST analysis of the 16S rDNA genes responsible for each representative profile made it possible to identify 27 genera distributed in three major phyla. In female mosquitoes, bacterial isolates were mostly Proteobacteria (51.3%) followed by Firmicutes (30.3%) and Actinobacteria (18.4%). Conversely, Actinobacteria was the most abundant phylum in male mosquitoes (48%) followed by Proteobacteria (30.6%) and Firmicutes (20.4%). The relative abundance and composition of isolates also varied between sampling sites, ranging from 3 distinct families in Ankazobe to 8 in Tsimbazaza Park, and Toamasina and Ambohidratrimo. Pantoea was the most common genus in both females and males from all sampling sites, except for Ambohidratrimo. No differences in genome size were found between Pantoea isolates from mosquitoes and reference strains in pulse field gel electrophoresis. However, according to the numbers and sizes of plasmids, mosquito isolates clustered into three different groups with other strains isolated from insects but distinct from isolates from the environment.
Conclusions
The recent upsurge in research into the functional role of the insect microbiota prompts the interest to better explore the role some bacteria detected here may have in the mosquito biology. Future studies of culturable bacteria might decipher whether they have a biological role in the invasiveness of Ae. albopictus. As a possible candidate for paratransgenesis, the predominant genus Pantoea will be characterized to better understand its genetic contents and any possible influence it may have on vector competence of Ae. albopictus.
【 授权许可】
2013 Valiente Moro et al.; licensee BioMed Central Ltd.
【 预 览 】
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20150330072113878.pdf | 567KB | download | |
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Figure 1. | 66KB | Image | download |
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【 参考文献 】
- [1]Rosenberg E, Zilber-Rosenberg I: Symbiosis and development: the hologenome concept. Birth Defects Res C Embryo Today 2011, 93(1):56-66.
- [2]Dillon R, Charnley K: Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res Microbiol 2002, 153:503-539.
- [3]Dillon RJ, Dillon VM: The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 2004, 49:71-92.
- [4]Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E: Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 2010, 107(46):20051-20056.
- [5]Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, Simon JC, Fukatsu T: Symbiotic bacterium modifies aphid body color. Science 2010, 330:1102-1104.
- [6]Toju H, Fukatsu T: Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol Ecol 2011, 20:853-868.
- [7]Pidiyar VJ, Jangid K, Patole MS, Shouche YS: Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus mosquito midgut based on 16 s ribosomal RNA gene analysis. AmJTrop Med Hyg 2004, 70:597-603.
- [8]Rani A, Sharma A, Rajagopal R, Adak T, Bhatnagar RK: Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiol 2009, 19(9):96.
- [9]Gusmão DS, Santos AV, Marini DC, Bacci M Jr, Berbert-Molina MA, Lemos FJ: Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Trop 2010, 115:275-281.
- [10]Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA, Mardani N, Ghoorchian S: Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: a step toward finding suitable paratransgenesis candidates. Acta Trop 2012, 121:129-134.
- [11]Dinparast Djadid N, Jazayeri H, Raz A, Favia G, Ricci I, Zakeri S: Identification of the midgut microbiota of An. stephensi and An. maculipennis for their application as a paratransgenic tool against malaria. PLoS One 2011, 6:e28484.
- [12]Zouache K, Raharimalala FN, Raquin V, Tran-Van V, Raveloson LHR, Ravelonandro P, Mavingui P: Bacterial diversity of field-caught mosquitoes, Aedes albopictus and Aedes aegypti, from different geographic regions of Madagascar. FEMS Microbiol Ecol 2011, 75:377-389.
- [13]Streit WR, Schmitz RA: Metagenomics-the key to the uncultured microbes. Curr Opin Microbiol 2004, 7(5):492-498.
- [14]Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, Nsango SE, Shahbazkia HR, 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 Patho 2012, 8(5):e1002742.
- [15]Schäfer A, Konrad R, Kuhnigk T, Kämpfer P, Hertel H, König H: Hemicellulose-degrading bacteria and yeasts from the termite gut. J Appl Bacteriol 1996, 80(5):471-478.
- [16]Watanabe Y, Shinzato N, Fukatsu T: Isolation of actinomycetes from termites’ guts. Biosci Biotechnol Biochem 2003, 7(8):1797-1801.
- [17]Moran NA, Baumann P: Bacterial endosymbionts in animals. Curr Opin Microbiol 2000, 3(3):270-275.
- [18]Pinto-Tomás AA, Anderson MA, Suen G, Stevenson DM, Chu FS, Cleland W, Weimer PJ, Currie CR: Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 2009, 326(5956):1120-1123.
- [19]Malhotra J, Dua A, Saxena A, Sangwan N, Mukherjee U, Pandey N, Rajagopal R, Khurana P, Khurana JP, Lal R: Genome sequence of Acinetobacter sp. strain HA, isolated from the gut of the polyphagous insect pest Helicoverpa armigera. J Bacteriol 2012, 194(18):5156.
- [20]Coutinho-Abreu IV, Zhu KY, Ramalho-Ortigao M: Transgenesis and paratransgenesis to control insect-borne diseases: current status and future challenges. Parasitol Int 2010, 59:1-8.
- [21]Favia G, Ricci I, Marzorati M, Negri I, Alma A, Sacchi L, Bandi C, Daffonchio D: Bacteria of the genus Asaia: a potential paratransgenic weapon against malaria. Adv Exp Med Biol 2008, 27:49-59.
- [22]Bisi DC, Lampe DJ: Secretion of anti-Plasmodium effector proteins from a natural Pantoea agglomerans isolate by using PelB and HlyA secretion signals. Appl Environ Microbiol 2011, 77:4669-4675.
- [23]Lambrechts L, Scott TW, Gubler DJ: Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission. PLoS Negl Trop Dis 2010, 25; 4(5):e646.
- [24]Ratsitorahina M, Harisoa J, Ratovonjato J, Biacabe S, Reynes JM, Zeller H, Raoelina Y, Talarmin A, Richard V, Louis Soares J: Outbreak of dengue and Chikungunya fevers, Toamasina, Madagascar, 2006. Emerging Infect Dis 2008, 14:1135-1137.
- [25]Renault P, Balleydier E, D’Ortenzio E, Bâville M, Filleul L: Epidemiology of chikungunya infection on Reunion Island, Mayotte, and neighboring countries. Med Mal Infect 2012, 42:93-101.
- [26]Minard G, Tran FH, Raharimalala FN, Hellard E, Ravelonandro P, Mavingui P, Valiente Moro C: Prevalence, genomic and metabolic profiles of Acinetobacter and Asaia associated with field-caught Aedes albopictus from Madagascar. FEMS Microbiol Ecol 2013, 83:63-73.
- [27]Raharimalala FN, Ravaomanarivo LH, Ravelonandro P, Rafarasoa LS, Zouache K, Tran-Van V, Mousson L, Failloux AB, Hellard E, Moro CV, Ralisoa BO, Mavingui P: Biogeography of the two major arbovirus mosquito vectors, Aedes aegypti and Aedes albopictus (Diptera, Culicidae), in Madagascar. Parasit Vectors 2012, 5:56. BioMed Central Full Text
- [28]Ravaonjanahary C: Les Aedes de Madagascar. France: Travaux et documents de 1′ORSTOM; 1978.
- [29]Bouvet PJM, Joly-Guillou ML: Acinetobacter. In Précis de bactériologie Clinique. Edited by Freney J, Renaud F, Hansen et W, Bollet C. Paris: Editions ESKA; 2000:1239-1258.
- [30]Mandel AD, Wright K, McKinnon JM: Selective medium for isolation of Mima and Herellea organisms. J Bacteriol 1964, 88:1524-1525.
- [31]Listiyanti P, Kawasaki H, Seki T, Yamoda Y, Chimura T, Komagata K: Identification of Acetobacter Strains isolated from Indonesian sources, and proposals of Acetobacter syzygii sp. nov., Acetobacter Cibinongensis sp.nov. Acetobacter cibinongensis sp. nov., and Acetobacter orientalis sp. J Gen Appl Microbiol 2001, 47:119-131.
- [32]Chouaia B, Rossi P, Montagna M, Ricci I, Crotti E, Damiani C, Epis S, Faye I, Sagnon N, Alma A, Favia G, Daffonchio D, Bandi C: Molecular evidence for multiple infections as revealed by typing of Asaia bacterial symbionts of four mosquito species. Appl Environ Microbiol 2010, 76:7444-7450.
- [33]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:95-98.
- [34]Schwartz DC, Cantor CR: Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell 1984, 37:67-75.
- [35]Eckhardt T: A rapid method for the identification of plasmid desoxyribonucleic acid in bacteria. Plasmid 1978, 1:584-588.
- [36]Mavingui P, Flores M, Guo X, Dávila G, Perret X, Broughton WJ, Palacios R: Dynamics of genome architecture in Rhizobium sp. strain NGR234. J Bacteriol 2002, 184:171-176.
- [37]Seifert H, Boullion B, Schulze A, Pulverer G: Plasmid DNA profiles of Acinetobacter baumannii: clinical application in a complex endemic setting. Infect Control Hosp Epidemiol 1994, 15:520-528.
- [38]Caballero-Mellado J, López-Reyes L, Bustillos R: Presence of 16S rRNA Genes in Multiple Replicons in Azospirillum brasilense. FEMS Microbial Lett 1999, 178:283-288.
- [39]Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G, Alexandre G, Sukharnikov LO, Wuichet K, Hurst GB, McDonald WH, Robertson JS, Barbe V, Calteau A, Rouy Z, Mangenot S, Prigent-Combaret C, Normand P, Boyer M, Siguier P, Dessaux Y, Elmerich C, Condemine G, Krishnen G, Kennedy I, Paterson AH, González V, Mavingui P, Zhulin IB: Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 2011, 7:e1002430.
- [40]R Development Core Team: R: A Language and Environment for Statistical computing. R Foundation for Statistical Computing, Vienna. 2009. Available at: http://www.R-project.org webcite
- [41]Lindh JM, Terenius O, Faye I: 16S rRNA gene-based identification of midgut bacteria from field-caught Anopheles gambiae sensu lato and A. funestus mosquitoes reveals new species related to known insect symbionts. Appl Environ Microbiol 2005, 71:7217-7223.
- [42]Terenius O, Lindh JM, Eriksson-Gonzales K, Bussière L, Laugen AT, Bergquist H, Titanji K, Faye I: Midgut bacterial dynamics in Aedes aegypti. FEMS Microbiol Ecol 2012, 80:556-565.
- [43]Müller GC, Xue RD, Schlein Y: Differential attraction of Aedes albopictus in the field to flowers, fruits and honeydew. Acta Trop 2011, 118:45-49.
- [44]Alvarez-Pérez S, Herrera CM, de Vega C: Zooming-in on floral nectar: a first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiol Ecol 2012, 80:591-602.
- [45]Gneiding K, Frodl R, Funke G: Identities of Microbacterium spp. encountered in human clinical specimens. J Clin Microbiol 2008, 46:3646-3652.
- [46]Helsel LO, Hollis D, Steigerwalt AG, Morey RE, Jordan J, Aye T, Radosevic J, Jannat-Khah D, Thiry D, Lonsway DR, Patel JB, Daneshvar MI, Levett PN: Identification of “Haematobacter” a new genus of aerobic Gram-negative rods isolated from clinical specimens, and reclassification of Rhodobacter massiliensis as “Haematobacter massiliensis comb. nov.”. J Clin Microbiol 2007, 45:1238-1243.
- [47]Brady C, Cleenwerck I, Venter S, Vancanneyt M, Swings J, Coutinho T: Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 2008, 31(6–8):447-460.
- [48]de Vries EJ, Jacobs G, Breeuwer JA: Growth and transmission of gut bacteria in the Western flower thrips. Frankliniella occidentalis. J Invertebr Pathol 2001, 77(2):129-137.
- [49]Straif SC, Mbogo CN, Toure AM, Walker ED, Kaufman M, Toure YT, Beier JC: Midgut bacteria in Anopheles gambiae and An. funestus (Diptera: Culicidae) from Kenya and Mali. J Med Entomol 1998, 35:222-226.
- [50]Riehle MA, Moreira CK, Lampe D, Lauzon C, Jacobs-Lorena M: Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int J Parasitol 2007, 37:595-603.
- [51]Joyce JD, Nogueira JR, Bales AA, Pittman KE, Anderson JR: Interactions between La Crosse virus and bacteria isolated from the digestive tract of Aedes albopictus (Diptera: Culicidae). J Med Entomol 2011, 48(2):389-94.