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Research article

Food Microbiology and Biotechnology (FMB)  |  Bioactive compounds and Physiological properties

Transcriptome Profiling and In Silico Analysis of the Antimicrobial Peptides of the Grasshopper Oxya chinensis sinuosa

In-Woo Kim 1, Kesavan Markkandan 2, Joon Ha Lee 1, Sathiyamoorthy Subramaniyam 2, Seungil Yoo 2, Junhyung Park 2 and Jae Sam Hwang 1*

1Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Republic of Korea, 2Theragen ETEX Bio Institute, Theragen Etex Inc., Suwon 16229, Republic of Korea

Received: August 11, 2016; Accepted: August 30, 2016

J. Microbiol. Biotechnol. 2016; 26(11): 1863-1870

Published November 28, 2016 https://doi.org/10.4014/jmb.1608.08029

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Antimicrobial peptides/proteins (AMPs) are present in all types of organisms, from microbes and plants to vertebrates and invertebrates such as insects. The grasshopper Oxya chinensis sinuosa is an insect species that is widely consumed around the world for its broad medicinal value. However, the lack of available genetic information for this species is an obstacle to understanding the full potential of its AMPs. Analysis of the O. chinensis sinuosa transcriptome and expression profile is essential for extending the available genetic information resources. In this study, we determined the whole-body transcriptome of O. chinensis sinuosa and analyzed the potential AMPs induced by bacterial immunization. A high-throughput RNA-Seq approach generated 94,348 contigs and 66,555 unigenes. Of these unigenes, 36,032 (54.14%) matched known proteins in the NCBI database in a BLAST search. Functional analysis demonstrated that 38,219 unigenes were clustered into 5,499 gene ontology terms. In addition, 26 cDNAs encoding novel AMPs were identified by an in silico approach using public databases. Our transcriptome dataset and AMP profile greatly improve our understanding of O. chinensis sinuosa genetics and provide a huge number of gene sequences for further study, including genes of known importance and genes of unknown function.

Keywords

Grasshopper, Oxya chinensis, Transcriptome, Antimicrobial peptides, Insect-derived AMP

References

  1. Azam I, Afsheen S, Zia A, Javed M, Saeed R, Sarwar MK, Munir B. 2015. Evaluating insects as bioindicators of heavy metal contamination and accumulation near industrial area of Gujrat, Pakistan. Biomed. Res. Int. 2015: 942751.
  2. Badisco L, Huybrechts J, Simonet G, Verlinden H, Marchal E, Huybrechts R, et al. 2011. Transcriptome analysis of the desert locust central nervous system: production and annotation of a Schistocerca gregaria EST database. PLoS One 6: e17274.
  3. Badman J, Harrison JF, McGarry MP. 2007. Grasshoppers in research and education: methods for maintenance and production. Lab Anim. (NY) 36: 27.
  4. Chen S, Yang P, Jiang F, Wei Y, Ma Z, Kang L. 2010. De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. PLoS One 5: e15633.
  5. Cherniack EP. 2010. Bugs as drugs, Part 1: Insects: the “new” alternative medicine for the 21st century. Altern. Med. Rev. 15: 124-135.
  6. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
  7. Costa-Neto EM. 2005. Entomotherapy, or the medicinal use of insects. J. Ethnobiol. 25: 93-114.
  8. Dang HX, Lawrence CB. 2014. Allerdictor: fast allergen prediction using text classification techniques. Bioinformatics 30: 1120-1128.
  9. Ganguly A, Chakravorty R, Sarkar A, Mandal DK, Haldar P, Ramos-Elorduy J, Moreno JMP. 2014. A preliminary study on Oxya fuscovittata (Marschall) as an alternative nutrient supplement in the diets of Poecillia sphenops (Valenciennes). PLoS One 9: e111848.
  10. Goodwin S, McPherson JD, McCombie WR. 2016. Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 17: 333-351.
  11. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. 2013. De novo transcript sequence reconstruction from RNA-Seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8: 1494-1512.
  12. Hadley EB, Hancock RE. 2010. Strategies for the discovery and advancement of novel cationic antimicrobial peptides. Curr. Top. Med. Chem. 10: 1872-1881.
  13. Huang Y, Niu B, Gao Y, Fu L, L i W. 2010. CD-HIT Suite: a Web server for clustering and comparing biological sequences. Bioinformatics 26: 680-682.
  14. Jin Y, Cong B, Wang L, Gao Y, Zhang H, Dong H, Lin Z. 2016. Differential gene expression analysis of the Epacromius coerulipes (Orthoptera: Acrididae) transcriptome. J. Insect Sci. 16: 42.
  15. Kim I-W, Lee JH, Subramaniyam S, Yun E-Y, Kim I, Park J, Hwang JS. 2016. De novo transcriptome analysis and detection of antimicrobial peptides of the American cockroach Periplaneta americana (Linnaeus). PLoS One 11: e0155304.
  16. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 1.
  17. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, et al. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346: 763-767.
  18. Mylonakis E, Podsiadlowski L, Muhammed M, Vilcinskas A. 2016. Diversity, evolution and medical applications of insect antimicrobial peptides. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371: 20150290.
  19. Van Huis A, Van Itterbeeck J, Klunder H, Mertens E, Halloran A, Muir G, Vantomme P. 2013. Edible Insects: Future Prospects for Food and Feed Security. FAO Forestry, Rome.
  20. Vilcinskas A. 2013. Evolutionary plasticity of insect immunity. J. Insect Physiol. 59: 123-129.
  21. Vilcinskas A, Mukherjee K, Vogel H. 2013. Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proc. Biol. Sci. 280: 20122113.
  22. Waghu F H, B arai R S, G urung P, Idicula-Thomas S. 2 015. CAMPR3: a database on sequences, structures and signatures of antimicrobial peptides. Nucleic Acids Res. 44: D1094D1097.
  23. Wang X, Fang X, Yang P, Jiang X, Jiang F, Zhao D, et al. 2014. The locust genome provides insight into swarm formation and long-distance flight. Nat. Commun. 5: 2957.
  24. Yan T, Yoo D, Berardini TZ, Mueller LA, Weems DC, Weng S, et al. 2005. PatMatch: a program for finding patterns in peptide and nucleotide sequences. Nucleic Acids Res. 33:W262-W266.
  25. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, et al. 2006. WEGO: a Web tool for plotting GO annotations. Nucleic Acids Res. 34: W293-W297.
  26. Zhang S, Pang B, Zhang L. 2015. Novel odorant-binding proteins and their expression patterns in grasshopper, Oedaleus asiaticus. Biochem. Biophys. Res. Commun. 460: 274-280.
  27. Zhang Y, Sun G, Yang M, Wu H, Zhang J, Song S, et al. 2011. Chronic accumulation of cadmium and its effects on antioxidant enzymes and malondialdehyde in Oxya chinensis (Orthoptera: Acridoidea). Ecotoxicol. Environ. Saf. 74: 1355-1362.

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(11): 1863-1870

Published online November 28, 2016 https://doi.org/10.4014/jmb.1608.08029

Copyright © The Korean Society for Microbiology and Biotechnology.

Transcriptome Profiling and In Silico Analysis of the Antimicrobial Peptides of the Grasshopper Oxya chinensis sinuosa

In-Woo Kim 1, Kesavan Markkandan 2, Joon Ha Lee 1, Sathiyamoorthy Subramaniyam 2, Seungil Yoo 2, Junhyung Park 2 and Jae Sam Hwang 1*

1Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Republic of Korea, 2Theragen ETEX Bio Institute, Theragen Etex Inc., Suwon 16229, Republic of Korea

Received: August 11, 2016; Accepted: August 30, 2016

Abstract

Antimicrobial peptides/proteins (AMPs) are present in all types of organisms, from microbes
and plants to vertebrates and invertebrates such as insects. The grasshopper Oxya chinensis
sinuosa is an insect species that is widely consumed around the world for its broad medicinal
value. However, the lack of available genetic information for this species is an obstacle to
understanding the full potential of its AMPs. Analysis of the O. chinensis sinuosa transcriptome
and expression profile is essential for extending the available genetic information resources. In
this study, we determined the whole-body transcriptome of O. chinensis sinuosa and analyzed
the potential AMPs induced by bacterial immunization. A high-throughput RNA-Seq
approach generated 94,348 contigs and 66,555 unigenes. Of these unigenes, 36,032 (54.14%)
matched known proteins in the NCBI database in a BLAST search. Functional analysis
demonstrated that 38,219 unigenes were clustered into 5,499 gene ontology terms. In addition,
26 cDNAs encoding novel AMPs were identified by an in silico approach using public
databases. Our transcriptome dataset and AMP profile greatly improve our understanding of
O. chinensis sinuosa genetics and provide a huge number of gene sequences for further study,
including genes of known importance and genes of unknown function.

Keywords: Grasshopper, Oxya chinensis, Transcriptome, Antimicrobial peptides, Insect-derived AMP

References

  1. Azam I, Afsheen S, Zia A, Javed M, Saeed R, Sarwar MK, Munir B. 2015. Evaluating insects as bioindicators of heavy metal contamination and accumulation near industrial area of Gujrat, Pakistan. Biomed. Res. Int. 2015: 942751.
  2. Badisco L, Huybrechts J, Simonet G, Verlinden H, Marchal E, Huybrechts R, et al. 2011. Transcriptome analysis of the desert locust central nervous system: production and annotation of a Schistocerca gregaria EST database. PLoS One 6: e17274.
  3. Badman J, Harrison JF, McGarry MP. 2007. Grasshoppers in research and education: methods for maintenance and production. Lab Anim. (NY) 36: 27.
  4. Chen S, Yang P, Jiang F, Wei Y, Ma Z, Kang L. 2010. De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. PLoS One 5: e15633.
  5. Cherniack EP. 2010. Bugs as drugs, Part 1: Insects: the “new” alternative medicine for the 21st century. Altern. Med. Rev. 15: 124-135.
  6. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
  7. Costa-Neto EM. 2005. Entomotherapy, or the medicinal use of insects. J. Ethnobiol. 25: 93-114.
  8. Dang HX, Lawrence CB. 2014. Allerdictor: fast allergen prediction using text classification techniques. Bioinformatics 30: 1120-1128.
  9. Ganguly A, Chakravorty R, Sarkar A, Mandal DK, Haldar P, Ramos-Elorduy J, Moreno JMP. 2014. A preliminary study on Oxya fuscovittata (Marschall) as an alternative nutrient supplement in the diets of Poecillia sphenops (Valenciennes). PLoS One 9: e111848.
  10. Goodwin S, McPherson JD, McCombie WR. 2016. Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 17: 333-351.
  11. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. 2013. De novo transcript sequence reconstruction from RNA-Seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8: 1494-1512.
  12. Hadley EB, Hancock RE. 2010. Strategies for the discovery and advancement of novel cationic antimicrobial peptides. Curr. Top. Med. Chem. 10: 1872-1881.
  13. Huang Y, Niu B, Gao Y, Fu L, L i W. 2010. CD-HIT Suite: a Web server for clustering and comparing biological sequences. Bioinformatics 26: 680-682.
  14. Jin Y, Cong B, Wang L, Gao Y, Zhang H, Dong H, Lin Z. 2016. Differential gene expression analysis of the Epacromius coerulipes (Orthoptera: Acrididae) transcriptome. J. Insect Sci. 16: 42.
  15. Kim I-W, Lee JH, Subramaniyam S, Yun E-Y, Kim I, Park J, Hwang JS. 2016. De novo transcriptome analysis and detection of antimicrobial peptides of the American cockroach Periplaneta americana (Linnaeus). PLoS One 11: e0155304.
  16. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 1.
  17. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, et al. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346: 763-767.
  18. Mylonakis E, Podsiadlowski L, Muhammed M, Vilcinskas A. 2016. Diversity, evolution and medical applications of insect antimicrobial peptides. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371: 20150290.
  19. Van Huis A, Van Itterbeeck J, Klunder H, Mertens E, Halloran A, Muir G, Vantomme P. 2013. Edible Insects: Future Prospects for Food and Feed Security. FAO Forestry, Rome.
  20. Vilcinskas A. 2013. Evolutionary plasticity of insect immunity. J. Insect Physiol. 59: 123-129.
  21. Vilcinskas A, Mukherjee K, Vogel H. 2013. Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proc. Biol. Sci. 280: 20122113.
  22. Waghu F H, B arai R S, G urung P, Idicula-Thomas S. 2 015. CAMPR3: a database on sequences, structures and signatures of antimicrobial peptides. Nucleic Acids Res. 44: D1094D1097.
  23. Wang X, Fang X, Yang P, Jiang X, Jiang F, Zhao D, et al. 2014. The locust genome provides insight into swarm formation and long-distance flight. Nat. Commun. 5: 2957.
  24. Yan T, Yoo D, Berardini TZ, Mueller LA, Weems DC, Weng S, et al. 2005. PatMatch: a program for finding patterns in peptide and nucleotide sequences. Nucleic Acids Res. 33:W262-W266.
  25. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, et al. 2006. WEGO: a Web tool for plotting GO annotations. Nucleic Acids Res. 34: W293-W297.
  26. Zhang S, Pang B, Zhang L. 2015. Novel odorant-binding proteins and their expression patterns in grasshopper, Oedaleus asiaticus. Biochem. Biophys. Res. Commun. 460: 274-280.
  27. Zhang Y, Sun G, Yang M, Wu H, Zhang J, Song S, et al. 2011. Chronic accumulation of cadmium and its effects on antioxidant enzymes and malondialdehyde in Oxya chinensis (Orthoptera: Acridoidea). Ecotoxicol. Environ. Saf. 74: 1355-1362.