期刊论文详细信息
BMC Research Notes
Analysis of the gut microbiota of walking sticks (Phasmatodea)
Chih-Horng Kuo3  Lynn S Kimsey1  Wen-Sui Lo2  Matan Shelomi1 
[1] Department of Entomology, University of California, Davis, USA;Graduate Institute of Biotechnology, National Chung Hsing University, Taichung, Taiwan;Biotechnology Center, National Chung Hsing University, Taichung, Taiwan
关键词: Digestive system;    Symbionts;    16S rDNA;    Microbiota;    Phasmatodea;   
Others  :  1141611
DOI  :  10.1186/1756-0500-6-368
 received in 2013-02-20, accepted in 2013-09-05,  发布年份 2013
PDF
【 摘 要 】

Background

Little is known about the Phasmatodea gut microbial community, including whether phasmids have symbiotic bacteria aiding in their digestion. While symbionts are near ubiquitous in herbivorous insects, the Phasmatodea’s distinctively thin body shape precludes the gut enlargements needed for microbial fermentation. High-throughput sequencing was used to characterize the entire microbiota of the fat bodies, salivary glands, and anterior and posterior midguts of two species of walking stick.

Results

Most bacterial sequences belonged to a strain of Spiroplasma (Tenericutes) found primarily in the posterior midgut of the parthenogenetic species Ramulus artemis (Phasmatidae). Beyond this, no significant differences were found between the R. artemis midgut sections or between that species and Peruphasma schultei (Pseudophasmatidae). Histological analysis further indicated a lack of bacteriocytes.

Conclusions

Phasmids are unlikely to depend on bacteria for digestion, suggesting they produce enzymes endogenously that most other herbivorous insects obtain from symbionts. This conclusion matches predictions based on phasmid anatomy. The role of Spiroplasma in insects warrants further study.

【 授权许可】

   
2013 Shelomi et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150327092551175.pdf 1075KB PDF download
Figure 6. 63KB Image download
Figure 5. 32KB Image download
Figure 4. 64KB Image download
Figure 3. 25KB Image download
Figure 2. 137KB Image download
Figure 1. 56KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】
  • [1]Buchner P: Endosymbiosis of Animals with Plant Microorganisms. New York: Interscience Publishers; 1965.
  • [2]Ishikawa H: Insect symbiosis: an introduction. In Insect Symbiosis. Edited by Bourtzis K, Miller TA. Boca Raton: CRC Press; 2003:1-21.
  • [3]Douglas AE: Buchnera bacteria and other symbionts of aphids. In Insect Symbiosis. Edited by Bourtzis K, Miller TA. Boca Raton: CRC Press; 2003:23-38.
  • [4]Lo N, Eggleton P: Termite phylogenetics and co-cladogenesis with symbionts. In Biology of Termites: A Modern Synthesis. Edited by Bignell DE, Roisin Y, Lo N. London: Springer; 2011:27-50.
  • [5]Douglas AE: Lessons from studying insect symbioses. Cell Host Microbe 2011, 10:359-367.
  • [6]Moran NA, McCutcheon JP, Nakabachi A: Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 2008, 42:165-190.
  • [7]Dharne M, Patole M, Shouche YS: Microbiology of the insect gut: tales from mosquitoes and bees. J Biosci 2006, 31:293-295.
  • [8]Moran NA, Hansen AK, Powell JE, Sabree ZL: Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One 2012, 7:e36393.
  • [9]Belda E, Pedrola L, Pereto J, Martinez-Blanch JF, Montagud A, Navarro E, Urchueguia J, Ramon D, Moya A, Porcar M: Microbial diversity in the midguts of field and lab-reared populations of the European corn borer Ostrinia nubilalis. PLoS One 2011, 6:e21751.
  • [10]Scharf ME, Tartar A: Termite digestomes as sources for novel lignocellulases. Biofuels, Bioprod Biorefin 2008, 2:540-552.
  • [11]Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernández M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR: Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 2007, 450:560-565.
  • [12]Watanabe H, Tokuda G: Cellulolytic systems in insects. Annu Rev Entomol 2010, 55:609-632.
  • [13]Shelomi M, Perkins LE, Cribb BW, Zalucki MP: Effects of leaf surfaces on first instar Helicoverpa armigera (Hübner)(Lepidoptera: Noctuidae) behaviour. Australian J Entomol 2010, 49:289-295.
  • [14]Wilson DB: Aerobic microbial cellulase systems. In Biomass Recalcitrance: Deconstructing the Plant Cell Wall for Bioenergy. Edited by Himmel ME. Oxford: Blackwell Publishing Ltd; 2008:374-392.
  • [15]Moran NA, Plague GR, Sandstrom JP, Wilcox JL: A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc Natl Acad Sci U S A 2003, 100(Suppl 2):14543-14548.
  • [16]Dowd PF: Symbiont-mediated detoxification in insect herbivores. In Microbial Mediation of Plant-Herbivore Interactions. Edited by Barbosa P, Krischik VA, Jones CG. New York City: John Wiley & Sons, Inc; 1991:411-440.
  • [17]Sabree ZL, Kambhampati S, Moran NA: Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci U S A 2009, 106:19521-19526.
  • [18]Idowua AB, Edemaa MO, Oyedepo MT: Extracellular enzyme production by microflora from the gut region of the variegated grasshopper Zonocerus variegatus (Orthoptera: Pyrgomorphidae). Int J Trop Insect Sci 2009, 29:229-235.
  • [19]Kaufman MG, Klug MJ: The contribution of hindgut bacteria to dietary carbohydrate utilization by crickets (Orthoptera: Gryllidae). Comp Biochem Physiol 1991, 98A:117-123.
  • [20]Mead LJ, Khachatourians GG, Jones GA: Microbial ecology of the gut in laboratory stocks of the migratory grasshopper, Melanoplus sanguinipes (Fab.) (Orthoptera: Acrididae). Appl Environ Microbiol 1988, 54:1174-1181.
  • [21]Cazemier AE, den Camp HJMO, Hackstein JHP, Vogels GD: Fibre digestion in arthropods. Comp Biochem Physiol 1997, 118A:101-109.
  • [22]DiBlasi E, Morse S, Mayberry JR, Avila LJ, Morando M, Dittmar K: New Spiroplasma in parasitic Leptus mites and their Agathemera walking stick hosts from Argentina. J Invertebr Pathol 2011, 107:225-228.
  • [23]Cameron AE: Structure of the alimentary canal of the stick-insect, Bacillus rossii Fabr.; with a note on the parthenogenesis of this species. Proc Zool Soc London 1912, 82:172-182.
  • [24]Chopard L: Ordre des Chéleutoptères. In Traité de Zoologie: Anatmie, Systématique, Biologie. Edited by Grassé P-P. Paris: Masson; 1949:594-617.
  • [25]Lasker R, Giese AC: Cellulose digestion by the silverfish Ctenolepisma Lineata. J Exp Biol 1940, 33:542-553.
  • [26]Coupland RE: Observations on the normal histology and histochemistry of the fat body of the locust (Schistocera gregaria). J Exp Biol 1957, 34:290-296.
  • [27]Gurr E: A Practical Manual of Medical and Biological Staining Techniques. New York: Interscience Publishers, Inc.; 1953.
  • [28]Ramsay JA: The excretory system of the stick insect Dixippus morosus (Orthoptera, Phasmidae). J Exp Biol 1955, 32:183-199.
  • [29]Chou HH, Holmes MH: DNA sequence quality trimming and vector removal. Bioinformatics 2001, 17:1093-1104.
  • [30]Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R: UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011, 27:2194-2200.
  • [31]Drancourt M, Raoult D: Sequence-based identification of new bacteria: a proposition for creation of an orphan bacterium repository. J Clin Microbiol 2005, 43:4311-4315.
  • [32]Janda JM, Abbott SL: 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol 2007, 45:2761-2764.
  • [33]Wang Q, Garrity GM, Tiedje JM, Cole JR: Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73:5261-5267.
  • [34]Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM: The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucl Acids Res 2009, 37:D141-D145.
  • [35]Ochman H, Worobey M, Kuo C-H, Ndjango J-BN, Peeters M, Hahn BH, Hugenholtz P: Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 2010, 8:e1000546.
  • [36]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
  • [37]Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden T: BLAST+: architecture and applications. BMC Bioinforma 2009, 10:421. BioMed Central Full Text
  • [38]Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW: GenBank. Nucl Acids Res 2012, 40:D48-D53.
  • [39]Hamady M, Lozupone C, Knight R: Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 2010, 4:17-27.
  • [40]Price MN, Dehal PS, Arkin AP: FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments. PLoS ONE 2010, 5:e9490.
  • [41]Suzuki R, Shimodaira H: Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 2006, 22:1540-1542.
  • [42]R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.
  • [43]Gasparich GE, Whitcomb RF, Dodge D, French FE, Glass J, Williamson DL: The genus Spiroplasma and its non-helical descendants: phylogenetic classification, correlation with phenotype and roots of the Mycoplasma mycoides clade. Int J Syst Evol Microbiol 2004, 54:893-918.
  • [44]Regassa LB, Gasparich GE: Spiroplasmas: evolutionary relationships and biodiversity. Front Biosci 2006, 11:2983-3002.
  • [45]Thakuria D, Schmidt O, Finan D, Egan D, Doohan FM: Gut wall bacteria of earthworms: a natural selection process. ISME J 2010, 4:357-366.
  • [46]Sun J-Z, Scharf ME: Exploring and integrating cellulolytic systems of insects to advance biofuel technology. Insect Sci 2010, 17:163-165.
  • [47]Flook PK, Rowell CHF: Inferences about orthopteroid phylogeny and molecular evolution from small subunit nuclear ribosomal DNA sequences. Insect Mol Biol 1998, 7:163-178.
  • [48]Jiggins FM, Hurst GD, Jiggins CD, Schulenburg JH VD, Majerus ME: The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitol 2000, 120:439-446.
  • [49]Huigens ME, Stouthamer R: Parthenogenesis associated with Wolbachia. In Insect Symbiosis. Edited by Bourtzis K, Miller TA. Boca Raton: CRC Press; 2003:247-266.
  • [50]More E: Parthenogenesis explained. Phasmid Studies 1996, 52:62-69.
  • [51]Singh A, Lal R: Sphingobium ummariense sp. nov., a hexachlorocyclohexane (HCH)-degrading bacterium, isolated from HCH-contaminated soil. Int J Syst Evol Microbiol 2009, 59:162-166.
  • [52]Ohmart CP, Thomas JR, Bubela B: Surfactant-producing microorganisms isolated from the gut of a Eucalyptus-feeding sawfly, Perga affinis affinis. Oecologia 1988, 77:140-142.
  文献评价指标  
  下载次数:48次 浏览次数:14次