Advertisement

Meta-omics in Detection of Silkworm Gut Microbiome Diversity

  • Mohanraj Ponnusamy
  • Chinnan Velmurugan Karthikeyan
  • Babu RamanathanEmail author
Chapter

Abstract

Insect gut symbiotic microbiota plays an essential role in the growth, development, pathogenesis, and environmental adaptation of host insects. As such, the molecular and systems level analysis of insect gut symbiotic microbial community may aid in discovery of novel biocatalysts for biomass deconstruction and to develop innovative strategies for pest management. In this review, we focused on understanding the current knowledge on investigation of insect gut microbes, especially in silkworms, and their functional role in the insect gut environment. Genome analysis has emerged as a major tool to study the composition, function, and evolution of various microbiota. We have particularly explored the use of metagenomics and metaproteomics in the field of studying insect gut microbiota and the recent advances in this field toward exploring the insect gut symbionts.

Keywords

Insect gut symbiotic Microbiota Gut microbes Metagenomics Metatranscriptomics 

References

  1. Adlakha N, Rajagopal R, Kumar S, Reddy VS, Yazdani SS (2011) Synthesis and characterization of chimeric proteins based on cellulase and xylanase from an insect gut bacterium. Appl Environ Microbiol 77:4859–4866PubMedPubMedCentralCrossRefGoogle Scholar
  2. Chen Q, Ma Z, Wang X, Li Z, Zhang Y, Ma S, Zhao P, Xia Q (2015) Comparative proteomic analysis of silkworm fat body after knocking out fibroin heavy chain gene: a novel insight into cross-talk between tissues. Funct Integr Genomics 15:611–637PubMedCrossRefPubMedCentralGoogle Scholar
  3. Cheng D, Guo Z, Riegler M, Xi Z, Liang G, Xu Y (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5:13PubMedPubMedCentralCrossRefGoogle Scholar
  4. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan P-L, Briese T, Hornig M, Geiser DM, Martinson V, vanEngelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M, Pettis JS, Lipkin WI (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283 LP–283287CrossRefGoogle Scholar
  5. Delahunty CM, Yates JR 3rd (2007) MudPIT: multidimensional protein identification technology. BioTechniques 43:563, 565, 567 passimGoogle Scholar
  6. Donini S, Garavaglia S, Ferraris DM, Miggiano R, Mori S, Shibayama K, Rizzi M (2017) Biochemical and structural investigations on phosphoribosylpyrophosphate synthetase from mycobacterium smegmatis. PLoS One 12:e0175815PubMedPubMedCentralCrossRefGoogle Scholar
  7. Dubey S, Avadhani K, Mutalik S, Sivadasan SM, Maiti B, Paul J, Girisha SK, Venugopal MN, Mutoloki S, Evensen Ø, Karunasagar I, Munang’andu HM (2016) Aeromonas hydrophila OmpW PLGA nanoparticle oral vaccine shows a dose-dependent protective immunity in Rohu (Labeo rohita). Vaccine 4:21CrossRefGoogle Scholar
  8. Eleftherianos L, Atri J, Accetta J, Castillo JC (2013) Endosymbiotic bacteria in insects: guardians of the immune system? Front Physiol 4. MAR:46PubMedPubMedCentralCrossRefGoogle Scholar
  9. Engel P, Moran NA (2013) The gut microbiota of insects – diversity in structure and function. FEMS Microbiol Rev 37:699–735PubMedCrossRefPubMedCentralGoogle Scholar
  10. Fruttero LL, Moyetta NR, Uberti AF, Coste Grahl MV, Lopes FC, Broll V, Feder D, Carlini CR (2016) Humoral and cellular immune responses induced by the urease-derived peptide Jaburetox in the model organism Rhodnius prolixus. Parasit Vectors 9:1–14CrossRefGoogle Scholar
  11. Geigenberger P, Thormählen I, Daloso DM, Fernie AR (2017) The unprecedented versatility of the plant thioredoxin system. Trends Plant Sci 22:249–262PubMedCrossRefPubMedCentralGoogle Scholar
  12. Giri SS, Sen SS, Jun JW, Sukumaran V, Park SC (2017) Role of Bacillus licheniformis VS16-derived biosurfactant in mediating immune responses in carp rohu and its application to the food industry. Front Microbiol 8:514PubMedPubMedCentralCrossRefGoogle Scholar
  13. Green JL, Bohannan BJM, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:1039–1043PubMedCrossRefPubMedCentralGoogle Scholar
  14. Grob C, Taubert M, Howat AM, Burns OJ, Dixon JL, Richnow HH, Jehmlich N, von Bergen M, Chen Y, Murrell JC (2015) Combining metagenomics with metaproteomics and stable isotope probing reveals metabolic pathways used by a naturally occurring marine methylotroph. Environ Microbiol 17:4007–4018PubMedCrossRefPubMedCentralGoogle Scholar
  15. Guo X, Dong Z, Zhang Y, Li Y, Liu H, Xia Q, Zhao P (2016) Proteins in the cocoon of silkworm inhibit the growth of Beauveria bassiana. PLoS One 11:e0151764PubMedPubMedCentralCrossRefGoogle Scholar
  16. Hongoh Y, Sharma VK, Prakash T, Noda S, Toh H, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M (2008) Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322:1108–1109PubMedCrossRefPubMedCentralGoogle Scholar
  17. Jiang L, Huang C, Sun Q, Guo H, Peng Z, Dang Y, Liu W, Xing D, Xu G, Zhao P, Xia Q (2015) Overexpression of host plant urease in transgenic silkworms. Mol Gen Genomics 290:1117–1123CrossRefGoogle Scholar
  18. Jiang P, Wei WF, Zhong GW, Zhou XG, Qiao WR, Fisher R, Lu L (2017) The function of the three phosphoribosyl pyrophosphate synthetase (Prs) genes in hyphal growth and conidiation in Aspergillus nidulans. Microbiology (United Kingdom) 163:218–232Google Scholar
  19. Luengo JM, García JL, Olivera ER (2001) The phenylacetyl-CoA catabolon: a complex catabolic unit with broad biotechnological applications. Mol Microbiol 39:1434–1442PubMedCrossRefPubMedCentralGoogle Scholar
  20. Madigan MT, Martinko JM, Bender KS, Buckley DH, Stahl DA (2015) Brock biology of microorganisms 14th edn. Pearson, BostonGoogle Scholar
  21. Miyashita A, Takahashi S, Ishii K, Sekimizu K, Kaito C (2015) Primed immune responses triggered by ingested bacteria lead to systemic infection tolerance in silkworms. PLoS One 10:1–14Google Scholar
  22. Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci 104:8627–8633PubMedCrossRefPubMedCentralGoogle Scholar
  23. Muturi EJ, Ramirez JL, Rooney AP, Kim C-H (2017) Comparative analysis of gut microbiota of mosquito communities in Central Illinois. PLoS Negl Trop Dis 11:e0005377PubMedPubMedCentralCrossRefGoogle Scholar
  24. Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI (2002) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32:777–784PubMedCrossRefPubMedCentralGoogle Scholar
  25. Nangia N, Kumar A, Nageshchandra BK (1999) Gut microflora of healthy mulberry silkworm, pp 247–150Google Scholar
  26. Nelson KE (2008) Metagenomics as a tool to study biodiversity. In: Accessing uncultivated microorganisms: from the environment to organisms and genomes and back, pp 153–170Google Scholar
  27. Ojeda V, Pérez-Ruiz JM, González M, Nájera VA, Sahrawy M, Serrato AJ, Geigenberger P, Cejudo FJ (2017) NADPH thioredoxin reductase C and thioredoxins act concertedly in seedling development. Plant Physiol 174:1436–1448PubMedPubMedCentralCrossRefGoogle Scholar
  28. Peterson BF, Scharf ME (2016) Metatranscriptome analysis reveals bacterial symbiont contributions to lower termite physiology and potential immune functions. BMC Genomics 17:772PubMedPubMedCentralCrossRefGoogle Scholar
  29. Ponnuvel KM, Nakazawa H, Furukawa S, Asaoka A, Ishibashi J, Tanaka H, Yamakawa M (2003) A lipase isolated from the silkworm Bombyx mori shows antiviral activity against nucleopolyhedrovirus. J Virol 77:10725–10729PubMedPubMedCentralCrossRefGoogle Scholar
  30. Potrikus CJ, Breznak JA (1980) Uric acid-degrading bacteria in guts of termites (Reticulitermes flavipes (Kollar)). Appl Environ Microbiol 40:117–124PubMedPubMedCentralGoogle Scholar
  31. Ramesha C, Lakshmi H, Kumari SS, Anuradha CM, Kumar CS (2012) Nutrigenetic screening strains of the mulberry silkworm, Bombyx mori, for nutritional efficiency. J Insect Sci 12:3CrossRefGoogle Scholar
  32. Roussel EG, Bonavita M-AC, Querellou J, Cragg BA, Webster G, Prieur D, Parkes RJ (2008) Extending the Sub-Sea-floor biosphere. Science 320:1046–1046PubMedCrossRefPubMedCentralGoogle Scholar
  33. Salem H, Kreutzer E, Sudakaran S, Kaltenpoth M (2013) Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environ Microbiol 15:1956–1968PubMedCrossRefPubMedCentralGoogle Scholar
  34. Schmeisser C, Steele H, Streit WR (2007) Metagenomics, biotechnology with non-culturable microbes. Appl Microbiol Biotechnol 75:955–962PubMedCrossRefPubMedCentralGoogle Scholar
  35. Shi W, Ding S-Y, Yuan JS (2011) Comparison of insect gut cellulase and xylanase activity across different insect species with distinct food sources. Bioenergy Res 4:1–10CrossRefGoogle Scholar
  36. Stepan’kov AA, Kuznetsova TA, Vecherskii MV (2017) Urease activity in the gastrointestinal tract of the European hare (Lepus europaeus). Biol Bull 44:224–227CrossRefGoogle Scholar
  37. Su LJ, Yang LL, Huang S, Su XQ, Li Y, Wang FQ, Wang ET, Kang N, Xu J, Song AD (2016) Comparative gut microbiomes of four species representing the higher and the lower termites. J Insect Sci (Online) 16.Google Scholar
  38. Sudakaran S, Salem H, Kost C, Kaltenpoth M (2012) Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Mol Ecol 21:6134–6151PubMedCrossRefPubMedCentralGoogle Scholar
  39. Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3:336–339PubMedPubMedCentralCrossRefGoogle Scholar
  40. Urakawa H, Kita-Tsukamoto K, Ohwada K (1999) Microbial diversity in marine sediments from Sagami Bay and Tokyo Bay, Japan, as determined by 16S rRNA gene analysis. Microbiology 145(Pt 1):3305–3315PubMedCrossRefPubMedCentralGoogle Scholar
  41. Vogel K, Blümer N, Korthals M, Mittelstädt J, Garn H, Ege M, von Mutius E, Gatermann S, Bufe A, Goldmann T, Schwaiger K, Renz H, Brandau S, Bauer J, Heine H, Holst O (2008) Animal shed Bacillus licheniformis spores possess allergy-protective as well as inflammatory properties. J Allergy Clin Immunol 122:307–312PubMedCrossRefPubMedCentralGoogle Scholar
  42. Warnecke F, Hugenholtz P (2007) Building on basic metagenomics with complementary technologies. Genome Biol 8:231PubMedPubMedCentralCrossRefGoogle Scholar
  43. Warnecke F, Luginbühl 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 (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565PubMedCrossRefPubMedCentralGoogle Scholar
  44. Wenzel M, Schönig I, Berchtold M, Kämpfer P (2002) Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J Appl Microbiol 92:32–40PubMedCrossRefPubMedCentralGoogle Scholar
  45. Wheeler MM, Zhou X, Scharf ME, Oi FM (2007) Molecular and biochemical markers for monitoring dynamic shifts of cellulolytic protozoa in Reticulitermes flavipes. Insect Biochem Mol Biol 37:1366–1374PubMedCrossRefPubMedCentralGoogle Scholar
  46. Zhou X, Smith JA, Oi FM, Koehler PG, Bennett GW, Scharf ME (2007) Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes. Gene 395:29–39PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Mohanraj Ponnusamy
    • 1
  • Chinnan Velmurugan Karthikeyan
    • 2
  • Babu Ramanathan
    • 3
    Email author
  1. 1.Department of SericultureForest College and Research Institute, Tamil Nadu Agricultural UniversityMettupalayamIndia
  2. 2.Department of BiotechnologyRVS Padmavathy College of HorticultureSempattiIndia
  3. 3.Department of Biological Sciences, School of Science and TechnologySunway UniversityKuala LumpurMalaysia

Personalised recommendations