Proteolytic activity of gut bacteria isolated from the velvet bean caterpillar Anticarsia gemmatalis

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 183, Issue 6, 2013, Pages 735-747

  Pilon, F M ^a   Visotto L E ^a   Guedes, R N C ^a   Oliveira, M G A ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

Bacteria symbionts; Bacteria insect non pathogenic interaction; Gut microbiota; Proteinase

Indexed keywords

CALCIUM CHLORIDE; CYSTEINE PROTEINASE; PROTEINASE INHIBITOR; SERINE PROTEINASE;

ANIMAL; ARTICLE; BACILLUS CEREUS; ENTEROCOCCUS; ENZYMOLOGY; GASTROINTESTINAL TRACT; KINETICS; METABOLISM; MICROBIOLOGY; MOTH; PH; STAPHYLOCOCCUS; SYMBIOSIS; TEMPERATURE;

ANIMALS; BACILLUS CEREUS; CALCIUM CHLORIDE; CYSTEINE PROTEASES; ENTEROCOCCUS; GASTROINTESTINAL TRACT; HYDROGEN-ION CONCENTRATION; KINETICS; MOTHS; PROTEASE INHIBITORS; SERINE PROTEASES; STAPHYLOCOCCUS; SYMBIOSIS; TEMPERATURE;

EID: 84880617595     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-013-0744-5     Document Type: Article

References (59)

1. Appel HM (1994) The chewing herbivore gut lumen: physicochemical conditions and their impact on plant nutrients, allelochemicals and insect pathogens. In: Bernays EA (ed) Insect-plant interactions, vol 5. CRC, Boca Raton, pp 209-221.
2. Beg QK, Gupta R (2003) Purification and characterization of an oxidation-stable, thiol-dependent serine alkaline protease from Bacillus mojavensis. Enz Microbl Technol 32: 294-304.
3. Bignell DE, Eggleton P (1995) On the elevated intestinal pH of higher termites (Isoptera, Termitidae). Insects Socieaux 42: 57-69.
4. Boulter D (1993) Insect pest control by copying nature using genetically engineering crops. Phytochemistry 34: 1453-1466.
5. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein dye binding. Anal Biochem 72: 248-254.
6. Broadway RM (1995) Are insects resistant to plant proteinase inhibitors? J Insect Physiol 41: 107-116.
7. Broadway RM (1996) Dietary proteinase inhibitors alter complement of midgut proteases. Arch Insect Biochem Physiol 32: 39-53.
8. Broadway RM, Duffey SS (1986) Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Helithis zea and Spodoptera exigua. J Insect Physiol 32: 39-53.
9. Carlini CR, Grossi-de-Sá MF (2002) Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon 40: 1515-1539.
10. Cooper J, Dobson H (2007) The benefits of pesticides to mankind and the environment. Crop Prot 26: 1337-1348.
11. D'Avila-Levy CM, Souza RF, Gomes RC, Vermelho AB, Branquinha MH (2003) A novel extracellular calcium-dependent cysteine proteinase from Crithidia deanei. Arch Biochem Biophys 420: 1-8.
12. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: non-pathogenic interactions. Annu Rev Entomol 49: 71-92.
13. Erlanger BF, Kokowsky N, Cohen W (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95: 271-278.
14. Gatehouse JA, Gatehouse AMR (1998) Identifying proteins with insecticidal activity: use of encoding genes to produce insect-resistant transgenic crops. Pestic Sci 52: 165-175.
15. Hilder VA, Boulter D (1999) Genetic engineering of crop plants for insect resistance-a critical review. Crop Prot 18: 177-191.
16. Hilder VA, Gatehouse AMR, Sheerman SE, Barker RF, Boulter D (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330: 160-163.
17. Hummel BCW (1959) A modified spectrophotometric determination of chymotrypsin, trypsin and thrombin. Can J Biochem Physiol 37: 1393-1399.
18. Indiragandhi P, Anandham R, Madhalyan M, Poonguzhali S, Kim GH, Saravanan VS, Sa T (2007) Cultivable bacteria associated with larval gut of prothiofos-resistant, prothiofos-susceptible and field-caught populations of diamondback moth, Plutella xylostella and their potential for antagonism towards entomopathogenic fungi and host insect nutrition. J Appl Microbiol 103: 2664-2675.
19. Indiraghandi P, Anandham R, Madhalyan M, Sa TM (2008) Characterization and plant growth-promoting traits of bacteria isolated from larval guts of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae). Curr Microbiol 56: 327-333.
20. Indiraghandi P, Yoon C, Yang JO, Cho S, Sa TM (2010) Microbial communities in the developmental stages of B and Q biotypes of sweetpotato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). J Korean Soc Appl Biol Chem 53: 605-617.
21. Institute SAS (2008) SAS/STAT user's guide. SAS Institute, Cary.
22. Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51: 45-66.
23. Jongsma MA, Bolter C (1997) The adaptation of insects to plant protease inhibitors. J Insect Physiol 43: 885-895.
24. Jongsma MA, Bakker PL, Peters J, Bosch D, Stickema WJ (1995) Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of proteinase activity insensitive to inhibition. Proc Natl Acad Sci USA 92: 8041-8045.
25. Joo HS, Kumar CG, Park GC, Kim KT, Paik SR, Chang CS (2002) Optimization of the production of an extracellular alkaline protease from Bacillus horikoshii. Proc Biochem 38: 155-159.
26. Kawalec M, Potempa JL, Moon JL, Travis J, Murray BE (2005) Molecular diversity of a putative virulence factor: purification and characterization of isoforms of an extracellular serine glutamyl endopeptidase of Enterococcus faecalis with different enzymatic activities. J Bacteriol 187: 266-275.
27. Laemmli UK (1970) Cleavage os structural protein during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
28. Marinho-Prado JS, Lourenção AL, Oliveira JA, Guedes RNC, Oliveira MGA (2011) Survival and feeding avoidance of the eucalyptus defoliator Thyrinteina arnobia exposed to the proteinase inhibitor berenil. J Appl Entomol 135: 763-770.
29. Matsumura F (2004) Contemporary issues on pesticide safety. J Pestic Sci 29: 299-303.
30. Matthews GA (2008) Attitudes and behaviors regarding use of crop protection products-a survey of more than 8500 smallholders in 26 countries. Crop Prot 27: 834-846.
31. Mendonça EG, Oliveira MGA, Visôtto LE, Guedes RNC (2012) Midgut cysteine-proteinase activity in the velvet bean caterpillar [Anticarsia gemmatalis (Hübner)]. J Pest Sci 85: 117-123.
32. Metcalf RL (1980) Changing role of insecticides in crop protection. Annu Rev Entomol 25: 219-256.
33. Mohamed SA, Fahmy AS, Mohamed TM, Hamdy SM (2005) Proteases in egg, miracidium and adult of Fasciola gigantic. Characterization of serine and cysteine proteases from adult. Comp Biochem Physiol B 142: 192-200.
34. Moreira LF, Campos WG, Ribeiro FR, Guedes RNC, Oliveira MGA (2011) Survival and developmental impairment induced by the trypsin inhibitor bis-benzamidine in the velvet bean caterpillar (Anticarsia gemmatalis). Crop Prot 30: 1285-1290.
35. Nicholson GM (2007) Fighting the global pest problem. Toxicon 49: 413-422.
36. Oliveira MGA, De Simone SG, Xavier LP, Guedes RNC (2005) Partial purification and characterization of digestive trypsin-like proteases from the velvet bean caterpillar, Anticarsia gemmatalis. Comp Biochem Physiol B 140: 369-380.
37. Pilon AM, Oliveira MGA, Guedes RNC (2006) Protein digestibility, protease activity, and post-embryonic development of the velvet bean caterpillar (Anticarsia gemmatalis) exposed to the trypsin-inhibitor benzamidine. Pestici Biochem Physiol 86: 23-29.
38. Pinto-Tomás AA, Sittenfeld A, Uribe-Lorío L, Chavarría F, Mora M, Janzen DH, Goodman RM, Simon HM (2011) Comparison of midgut bacterial diversity in tropical caterpillars (Lepidoptera: Saturniidae) fed o different diets. Environ Entomol 40: 1111-1122.
39. Pompermayer P, Lopes AR, Parra JRP, Terra WR, Silva-Filho M (2001) Effects of soybean proteinase inhibitor on development, survival and reproductive potential of the sugarcane borer, Diatraea saccharalis. Entomol Exp Appl 99: 79-85.
40. Rao MB, Aparna MT, Ghatge MS, Deshpande VV (1998) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62: 597-635.
41. Reeck GR, Oppert B, Denton M, Kanost M, Baker JE, Kramer KJ (1999) Insect proteinases. In: Truk V (ed) Proteases: new perspectives. Birkhausser, Boston, pp 125-148.
42. Rosell G, Quero C, Coll J, Guerrero A (2008) Biorational insecticides in pest management. J Pestic Sci 33: 103-121.
43. Shaw E, Mares-Guia M, Cohen W (1965) Evidence for na active center histidine in trypsin with the use of a specific reagent, 1-chloro-3-tosylamido-7-amino-2-heptanone, the chloromethyl ketone derived from N-alpha-tosyl-l-lysine. Biochemistry 4: 2219-2224.
44. Silva LB, Reis AP, Pereira EJG, Oliveira MGA, Guedes RNC (2010a) Altered cysteine-proteinase activity in insecticide-resistant and -susceptible strains of the maize weevil, Sitophilus zeamais. Comp Biochem Physiol B 157: 80-87.
45. Silva LB, Reis AP, Pereira EJG, Oliveira MGA, Guedes RNC (2010b) Partial purification and characterization of trypsin-like proteinases from insecticide-resistant and -susceptible strains of the maize weevil, Sitophilus zeamais. Comp Biochem Physiol B 155: 12-19.
46. Silva-Lopez RE, De Simone SG (2004) Leishmania (Leishmania) amazonensisi: purification and characterization of a promastigote serine protease. Exp Parasitol 107: 173-182.
47. Sipos T, Merkel JR (1970) Na effect of calcium ions on the activity, heat stability, and structure of trypsin. Biochemistry 9: 2766-2775.
48. Stotz HU, Kroymann J, Mitchell-Olds T (1999) Plant-insect interactions. Cur Opin Plant Biol 2: 268-272.
49. Systat 2008. SigmaPlot v.10 user's guide. Systat Software, Chicago.
50. Terra WR, Ferreira C (2005) Biochemistry and digestion. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol 4. Pergamon, New York, pp 171-224.
51. Vajda T, Garai A (1981) Comparison of the effect of calcium (II) and manganese (II) ions on trypsin autolysis. J Inorg Biochem 15: 307-315.
52. Valasaki K, Staikou A, Theodorou LG, Charamopoulou V, Zacharaki P, Papamichael EM (2008) Purification and kinetics of two novel thermophilic extracellular proteases from Lactobacillus helveticus, from kefir with possible biotechnological interest. Biores Technol 99: 5804-5813.
53. Visôtto LE, Oliveira MGA, Guedes RNC, Ribon AOB, Good-God PIV (2009a) Contribution of gut bacteria to digestion and development of the velvet bean caterpillar, Anticarsia gemmatalis. J Insect Physiol 55: 185-191.
54. Visôtto LE, Oliveira MGA, Ribon AOB, Mares-Guia TR, Guedes RNC (2009b) Characterization and identification of proteolytic bacteria from the gut of the velvet bean caterpillar (Lepidoptera: Noctuidae). Environ Entomol 38: 1078-1085.
55. Walenciak O, Zwisler W, Gross EM (2002) Influence of myriophyllum spicatum-derived tannins on gut microbiota of its herbivore Acenria ephemerella. J Chem Ecol 28: 2045-2056.
56. Walker AJ, Glen DM, Shewry PR (1999) Bacteria associated with the digestive system of the slug Deroceras reticulatumi are not required for protein digestion. Soil Biol Biochem 31: 1387-1394.
57. Wang SL, Chen YH, Wang CL, Yen YH, Chern MK (2005) Purification and characterization of a serine protease extracellularly produced by Aspergillus fumigates in a shrimp and crab shell powder medium. Enz Microb Technol 36: 660-665.
58. Xavier LP, Oliviera MGA, Guedes RNC, Santos AV, De Simone SG (2005) Trypsin-like activity of membrane-bound midgut proteases from Anticarsia gemmatalis (Lepidoptera: Noctuidae). Eur J Entomol 102: 147-153.
59. Zaspel JM, Hoy MA (2008) Microbial diversity associated with the fruit-piercing and blood-feeding moth Calyptra thalictri (Lepidoptera: Noctuidae). An Entomol Soc Am 101: 1050-1055.