BMC Microbiology | |
The gut microbiota of larvae of Rhynchophorus ferrugineus Oliver (Coleoptera: Curculionidae) | |
Paola Quatrini3  Simone Cappello1  Barbara Manachini3  Enzo Messina1  Marcello Tagliavia2  | |
[1] Istituto per l’Ambiente Marino Costiero (C.N.R. – IAMC) U.O.S. di Messina, Spianata S. Raineri, 86, Messina 98122, Italy;Istituto per l’Ambiente Marino Costiero (C.N.R. – IAMC) U.O.S. di Capo Granitola, Via del Mare, 3 Torretta-Granitola, Mazara, TP 91021, Italy;Department STEBICEF, University of Palermo Viale delle Scienze Ed.16, Palermo 90128, Italy | |
关键词: Pyrosequencing; TTGE; Dysgonomonas; Enterobacteriaceae; | |
Others : 1141026 DOI : 10.1186/1471-2180-14-136 |
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received in 2013-12-09, accepted in 2014-04-25, 发布年份 2014 | |
【 摘 要 】
Background
The red palm weevil (RPW) Rhynchophorus ferrugineus Olivier (Coleoptera: Curculionidae) is one of the major pests of palms. The larvae bore into the palm trunk and feed on the palm tender tissues and sap, leading the host tree to death. The gut microbiota of insects plays a remarkable role in the host life and understanding the relationship dynamics between insects and their microbiota may improve the biological control of insect pests. The purpose of this study was to analyse the diversity of the gut microbiota of field-caught RPW larvae sampled in Sicily (Italy).
Results
The 16S rRNA gene-based Temporal Thermal Gradient Gel Electrophoresis (TTGE) of the gut microbiota of RPW field-trapped larvae revealed low bacterial diversity and stability of the community over seasons and among pools of larvae from different host trees. Pyrosequencing of the 16S rRNA gene V3 region confirmed low complexity and assigned 98% of the 75,564 reads to only three phyla: Proteobacteria (64.7%) Bacteroidetes (23.6%) and Firmicutes (9.6%) and three main families [Enterobacteriaceae (61.5%), Porphyromonadaceae (22.1%) and Streptococcaceae (8.9%)]. More than half of the reads could be classified at the genus level and eight bacterial genera were detected in the larval RPW gut at an abundance ≥1%: Dysgonomonas (21.8%), Lactococcus (8.9%), Salmonella (6.8%), Enterobacter (3.8%), Budvicia (2.8%), Entomoplasma (1.4%), Bacteroides (1.3%) and Comamonas (1%). High abundance of Enterobacteriaceae was also detected by culturing under aerobic conditions. Unexpectedly, acetic acid bacteria (AAB), that are known to establish symbiotic associations with insects relying on sugar-based diets, were not detected.
Conclusions
The RPW gut microbiota is composed mainly of facultative and obligate anaerobic bacteria with a fermentative metabolism. These bacteria are supposedly responsible for palm tissue fermentation in the tunnels where RPW larvae thrive and might have a key role in the insect nutrition, and other functions that need to be investigated.
【 授权许可】
2014 Tagliavia et al.; licensee BioMed Central Ltd.
【 预 览 】
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Figure 1. | 65KB | Image | download |
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【 参考文献 】
- [1]Cox ML: Red palm weevil, Rhynchophorus ferrugineus in Egypt. FAO Pl Prot Bul 1993, 41:30-31.
- [2]Butera G, Ferraro C, Colazza S, Alonzo G, Quatrini P: The culturable bacterial community of frass produced by larvae of Rhynchophorus ferrugineus Olivier (Coleoptera: Curculionidae) in the Canary island date palm. Lett Appl Microbiol 2012, 54:530-536.
- [3]Dembilio Ó, Jacas JA: Basic bio-ecological parameters of the invasive Red Palm Weevil, Rhynchophorus ferrugineus (Coleoptera: Curculionidae), in Phoenix canariensis under Mediterranean climate. Bull Entomol Res 2011, 101:153-163.
- [4]Faleiro JR: A review on the issues and management of red palm weevil Rhynchophorus ferrugineus (Coleoptera: Rhynchophoridae) in coconut and date palm during the last one hundred years. Internat J Trop Insect Sci 2006, 26:135-154.
- [5]Ferry M, Gomez S: The Red Palm Weevil in the Mediterranean area. Palms 2002, 46:172-178.
- [6]Engel P, Moran NA: The gut microbiota of insects - diversity in structure and function. FEMS Microbiol Rev 2013, 37:699-735.
- [7]Hongoh Y: Diversity and genomes of uncultured microbial symbionts in the termite gut. Biosci Biotechnol Biochem 2010, 74:1145-1151.
- [8]Colman DR, Toolson EC, Takacs-Vesbach CD: Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol 2012, 21:5124-5137.
- [9]Rosenberg E, Zilber-Rosenberg I: Symbiosis and development: the hologenome concept. Birth Defects Res (Part C) 2011, 93:56-66.
- [10]Dillon RJ, Dillon VM: The gut bacteria of insects: non-pathogenic interactions. Annu Rev Entomol 2004, 49:71-92.
- [11]Kaufman MG, Klug MJ: The contribution of hindgut bacteria to dietary carbohydrate utilization by crickets (Orthoptera, Gryllidae). Comp Biochem Physiol A Physiol 1991, 98:117-123.
- [12]Chakravorty S, Helb D, Burday M, Connell N, Alland D: A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J Microbiol Methods 2007, 69:330-339.
- [13]Tang X, Freitak D, Vogel H, Ping L, Shao Y, Cordero EA, Andersen G, Westermann M, Heckel DG, Boland W: Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS One 2012, 7(7):e36978. doi:10.1371/journal.pone.0036978
- [14]Shivaji S, Chaturvedi P, Suresh K, Reddy GS, Dutt CB, Wainwright M, Narlikar JV, Bhargava PM: Bacillus aerius sp. nov., Bacillus aerophilus sp. nov., Bacillus stratosphericus sp. nov. and Bacillus altitudinis sp. nov., isolated from cryogenic tubes used for collecting air samples from high altitudes. Int J Syst Evol Microbiol 2006, 56:1465-1473.
- [15]Suzuki T, Yamasato K: Phylogeny of spore-forming lactic acid bacteria based on 16S rRNA gene sequences. FEMS Microbiol Lett 1994, 115:13-17.
- [16]Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, Alma A, Sacchi L, Bourtzis K, Mandrioli M, Cherif A, Bandi C, Daffonchio D: Acetic acid bacteria, newly emerging symbionts of insects. Appl Environ Microbiol 2010, 76:6963-6970.
- [17]Claesson MJ, Wang QO, O’Sullivan O, Greene-Diniz R, Cole JR, Ross RP, O’Toole PW: Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Res 2010, 38(22):e200. doi:10.1093/nar/gkq873
- [18]Milani C, Hevia A, Foroni E, Duranti S, Turroni F, Lugli A, Sanchez B, Martìn R, Gueimonde M, van Sinderen D, Margolles A, Ventura M: Assessing the fecal microbiota: an optimized ion torrent 16S rRNA gene-based analysis protocol. PLoS One 2013, 8(7):e68739. doi:10.1371/journal.pone.0068739
- [19]Youssef N, Sheik CS, Krumholz LR, Najar FZ, Roe BA, Elshahed MS: Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl Environ Microbiol 2009, 75:5227-5236.
- [20]Morales-Jiménez J, Zuniga G, Villa-Tanaca L, Hernandez-Rodriguez C: Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae: Scolytinae). Microb Ecol 2009, 58:879-891.
- [21]Chandler JA, Morgan Lang J, Bhatnagar S, Eisen JA, Kopp : A bacterial communities of diverse drosophila species: ecological context of a host–microbe model system. PLoS Genet 2011, 7(9):e1002272. doi:10.1371/journal.pgen.1002272
- [22]Nagnan P, Cain AH, Rochat D: Extraction et identification des composés volatils de la sève de palmier à huile fermentée (vin de palme) attractifs potentiels pour le charancon du palmier. Oléagineux 1992, 47:135-142.
- [23]Behar A, Yuval B, Jurkevitch E: Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol Ecol 2005, 14:2637-2643.
- [24]Chandrasekhar K, Sreevani S, Seshapani P, Pramodhakumari J: A Review on palm wine. J Res Biol Sci 2012, 2(1):33-38.
- [25]Santo Domingo JW, Kaufman MG, Klug MJ, Tiedje JM: Characterization of the cricket hindgut microbiota with fluorescently labeled rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 1998, 64:752-755.
- [26]Wong CN, Ng P, Douglas AE: Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ Microbiol 2011, 13:1889-1900.
- [27]Mazza G, Arizza V, Baracchi D, Barzanti GP, Benvenuti C, Francardi V, Frandi A, Gherardi F, Longo S, Manachini B, Perito B, Rumine P, Schillaci D, Turillazzi S, Cervo R: Antimicrobial activity of the red palm weevil Rhynchophorus ferrugineus. Bull Insectol 2011, 64:33-41.
- [28]Rinke R, Costa AS, Fonseca FP, Almeida LC, Delalibera Júnior I, Henrique-Silva F: Microbial diversity in the larval gut of field and laboratory populations of the sugarcane weevil Sphenophorus levis (Coleoptera, Curculionidae). Genet Mol Res 2011, 10:2679-2691.
- [29]Hofstad T, Olsen I, Eribe ER, Falsen E, Collins MD, Lawson PA: Dysgonomonas gen. nov. to accommodate Dysgonomonas gadei sp. nov., an organism isolated from a human gall bladder, and Dysgonomonas capnocytophagoides (formerly CDC group DF-3). Int J Syst Evol Microbiol 2000, 50:2189-2195.
- [30]Watanabe K, Miyahara M, Shimoyama T, Hashimoto K: Population dynamics and current-generation mechanisms in cassette-electrode microbial fuel cells. Appl Microbiol Biotechnol 2011, 92:1307-1314.
- [31]Gupta AK, Nayduch D, Verma P, Shah B, Ghate HV, Patole MS, Shouche YS: Phylogenetic characterization of bacteria in the gut of house flies (Musca domestica L.). FEMS Microbiol Ecol 2012, 79:581-593.
- [32]Campbell BC, Bragg TS, Turner CE: Phylogeny of symbiotic bacteria of four weevil species (Coleoptera:Curculionidae) based on analysis of 16S ribosomal DNA. Insect Biochem Molec Biol 1992, 22:415-421.
- [33]Tully JG, Whitcomb RF, Hackett KJ, Williamson DL, Laigret F, Carle P, Bové JM, Henegar RB, Ellis NM, Dodge DE, Adams J: Entomoplasma freundtii sp. nov., a new species from a green tiger beetle (Coleoptera: Cicindelidae). Int J Syst Bacteriol 1998, 48:1197-1204.
- [34]Yu H, Wang Z, Liu L, Xia Y, Cao Y, Yin Y: Analysis of the intestinal microflora in Hepialus gonggaensis larvae using 16S rRNA sequences. Curr Microbiol 2008, 56:391-396.
- [35]Suen G, Scott JJ, Aylward FO, Adams SM, Tringe SG, Pinto-Tomás AA, Foster CE, Pauly M, Weimer PJ, Barry KW, Goodwin LA, Bouffard P, Li L, Osterberger J, Harkins TT, Slater SC, Donohue TJ, Currie CR: An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genet 2010, 6(9):e1001129. doi:10.1371/journal.pgen.1001129
- [36]Paoletti MG, Mazzon L, Martinez-Sañudo I, Simonato M, Beggio M, Dreon AL, Pamio A, Brilli M, Dorigo L, Engel AS, Tondello A, Baldan B, Concheri G, Squartini A: A unique midgut-associated bacterial community hosted by the cave beetle Cansiliella servadeii (Coleoptera: Leptodirini) reveals parallel phylogenetic divergences from universal gut-specific ancestors. BMC Microbiol 2013, 13:129. BioMed Central Full Text
- [37]Guarino S, Lo Bue P, Peri E, Colazza S: Responses of Rhynchophorus ferrugineus adults to selected synthetic palm esters: electroantennographic studies and trap catches in an urban environment. Pest Manag Sci 2011, 67:77-81.
- [38]Broderick NA, Goodman RM, Handelsman J, Raffa KF: Effect of host diet and insect source on synergy of gypsy moth (Lepidoptera: Lymantriidae) mortality to Bacillus thuringiensis subsp. kurstaki by zwittermicin A. Environ Entomol 2003, 32:387-391.
- [39]Abe F, Ohkusu M, Kawamoto S, Sone K, Hata K: Isolation of yeasts from palm tissues damaged by the red palm weevil and their possible effect on the weevil overwintering. Mycoscience 2010, 51:215-223.
- [40]Hassan AA, Akineden O, Kress C, Estuningsih S, Schneider E, Usleber E: Characterization of the gene encoding the 16S rRNA of Enterobacter sakazakii and development of a species-specific PCR method. Int J Food Microbiol 2007, 116:214-220.
- [41]Toledo AV, Alippi AM, de Remes Lenicov AM: Growth inhibition of Beauveria bassiana by bacteria isolated from the cuticular surface of the corn leafhopper, Dalbulus maidis and the planthopper, Delphacodes kuscheli, two important vectors of maize pathogens. J Insect Sci 2011, 11:1-13.
- [42]Yamada Y, Katsura K, Kawasaki H, Widyastuti Y, Saono S, Seki T, Uchimura T, Komagata K: Asaia bogorensis gen. nov., sp. nov., an unusual acetic acid bacterium in the alpha-Proteobacteria. Int J Syst Evol Microbiol 2000, 50:823-829.
- [43]Doolittle M, Raina A, Lax A, Boopathy R: Presence of nitrogen fixing Klebsiella pneumoniae in the gut of the Formosan subterranean termite (Coptotermes formosanus). Bioresour Technol 2008, 99:3297-3300.
- [44]Pittman GW, Brumbley SM, Allsopp PG, O’Neill SL: “Endomicrobia” and other bacteria associated with the hindgut of Dermolepida albohirtum larvae. Appl Environ Microbiol 2008, 74:762-767.
- [45]Muyzer G, DeWaal EC, Uitterlinden AG: Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 1993, 59:695-700.
- [46]Hamady M, Walker JJ, Harris JH, Gold NJ, Knight R: Error-correcting barcoded primers allow hundreds of samples to be pyrosequenced in multiplex. Nat Methods 2008, 5:235-237.
- [47]Niu B, Fu L, Sun S, Li W: Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinforma 2010, 13:11-187.
- [48]Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM: Ribosomal database project: data and tools for high throughput rRNA analysis. Nucl Acids Res 2014, 41(Database issue):D633-D642. doi:10.1093/nar/gkt1244
- [49]Pruesse E, Peplies J, Glöckner FO: SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012, 28:1823-1829.
- [50]Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar , Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH: ARB: a software environment for sequence data. Nucleic Acids Res 2004, 32:1363-1371.
- [51]Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ: At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 2005, 71:7724-7736.
- [52]Entsminger GL: EcoSim Professional: Null Modelling Software for Ecologists, Version 1. Acquired Intelligence Inc., Kesey-Bear, & Pinyon Publishing; 2012. http://garyentsminger.com/ecosim/index.htm webcite
- [53]Weisburg WG, Barns SM, Pelletier DA, Lane DJ: 16S Ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991, 173:697-703.
- [54]Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO: SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007, 35:7188-7196.
- [55]Jia S, Zhang X, Zhang G, Yin A, Zhang S, Li F, Wang L, Zhao D, Yun Q, Tala , Wang J, Sun G, Baabdullah M, Yu X, Hu S, Al-Mssallem IS, Yu J: Seasonally variable intestinal metagenomes of the red palm weevil (Rhynchophorus ferrugineus). Environ Microbiol 2013, 15:3020-3029.