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Lysinabacillus fusiformis and Paenibacillus alvei Obtained from the Internal of NasutitermesTermites Revealed Their Ability as Antagonist of Plant Pathogenic Fungi

  • Fitriana, Yuyun (Department of Plant Protection, Faculty of Agriculture, University of Lampung) ;
  • Tampubolon, Desi Apriani Teresa (Department of Agrotechnology, Faculty of Agriculture, University of Lampung) ;
  • Suharjo, Radix (Department of Plant Protection, Faculty of Agriculture, University of Lampung) ;
  • Lestari, Puji (Department of Plant Protection, Faculty of Agriculture, University of Lampung) ;
  • Swibawa, I Gede (Department of Plant Protection, Faculty of Agriculture, University of Lampung)
  • Received : 2022.03.07
  • Accepted : 2022.07.17
  • Published : 2022.10.01

Abstract

This study was performed to reveal phenotypic characters and identity of symbiont bacteria of Nasutitermes as well as investigate their potential as antagonist of plant pathogenic fungi. Isolation of the symbiont bacteria was carried out from inside the heads and the bodies of soldier and worker termite which were collected from 3 locations of nests. Identification was performed using phenotypic test and sequence of 16S ribosomal DNA (16S rDNA). Antagonistic capability was investigated in the laboratory against 3 phytopathogenic fungi i.e., Phytophthora capsici, Ganoderma boninense, and Rigidoporus microporus. Totally, 39 bacterial isolates were obtained from inside the heads and the bodies of Nasutitermes. All the isolates showed capability to inhibit growth of P. capsici, however, 34 isolates showed capability to inhibit growth of G. boninense and 32 isolates showed capability to inhibit growth of R. microporus. Two bacterial strains (IK3.1P and 1B1.2P) which showed the highest percentage of inhibition were further identified based on their sequence of 16S rDNA. The result showed that 1K3.1P strain was placed in the group of type strain and reference strains of Lysinibacillus fusiformis meanwhile 1B1.2P strain was grouped within type strain and reference strains Paenibacillus alvei. The result of this study supply valuable information on the role of symbiont bacteria of Nasutitermes, which may support the development of the control method of the three above-mentioned phytopathogenic fungi.

Keywords

Acknowledgement

This work was supported by Daftar Isian Pelaksanaan Anggaran (DIPA) Badan Layanan Umum (BLU) University of Lampung through fundamental research grant No. 1604/UN26.21/PN/2021. We thanks to Faculty of Agriculture, University of Lampung for permitting us using research facilities during this study.

References

  1. Adeolu, M., Alnajar, S., Naushad, S. and Gupta, R. S. 2016. Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int. J. Syst. Evol. Microbiol. 66:5575-5599. https://doi.org/10.1099/ijsem.0.001485
  2. Ahmad, F., Fouad, H., Liang, S.-Y., Hu, Y. and Mo, J.-C. 2021. Termites and Chinese agricultural system: applications and advances in integrated termite management and chemical control. Insect Sci. 28:2-20. https://doi.org/10.1111/1744-7917.12726
  3. Ahmed, I., Yokota, A., Yamazoe, A. and Fujiwara, T. 2007. Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. Int. J. Syst. Evol. Microbiol. 57:1117-1125. https://doi.org/10.1099/ijs.0.63867-0
  4. Antonopoulos, D. F., Tjamos, S. E., Antoniou, P. P., Rafeletos, P. and Tjamos, E. C. 2008. Effect of Paenibacillus alvei, strain K165, on the germination of Verticillium dahliae microsclerotia in planta. Biol. Control 46:166-170. https://doi.org/10.1016/j.biocontrol.2008.05.003
  5. Atanasova-Pancevska, N. and Kungulovski, D. 2018. In vitro potential of Paenibacillus alvei DZ-3 as a biocontrol agent against several phytopathogenic fungi. Biologija 64:65-72.
  6. Berasategui, A., Shukla, S., Salem, H. and Kaltenpoth, M. 2016. Potential applications of insect symbionts in biotechnology. Appl. Microbiol. Biotechnol. 100:1567-1577. https://doi.org/10.1007/s00253-015-7186-9
  7. Brune, A. 2013. Symbiotic associations between termites and prokaryotes. In: The prokaryotes: prokaryotic biology and symbiotic associations, eds. by E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt and F. Thompson, pp. 545-577. Springer-Verlag, Berlin, Germany.
  8. Butera, G., Ferraro, C., Alonzo, G., Colazza, S. and Quatrini, P. 2016. The gut microbiota of the wood-feeding termite Reticulitermes lucifugus (Isoptera; Rhinotermitidae). Ann. Microbiol. 66:253-260. https://doi.org/10.1007/s13213-015-1101-6
  9. Cardoso, J. E. and Echandi, E. 1987. Biological control of Rhizoctonia root rot of snap bean with binucleate Rhizoctonialike fungi. Plant Dis. 71:167-170. https://doi.org/10.1094/PD-71-0167
  10. Cardoza, Y. J., Klepzig, K. D. and Raffa, K. F. 2006. Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol. 31:636-645. https://doi.org/10.1111/j.1365-2311.2006.00829.x
  11. Charkowski, A. O. 2018. The changing face of bacterial soft-rot diseases. Annu. Rev. Phytopathol. 56:269-288. https://doi.org/10.1146/annurev-phyto-080417-045906
  12. Cohen, I., Ron, I. G. and Ben-Jacob, E. 2000. From branching to nebula patterning during colonial development of the Paenibacillus alvei bacteria. Physica A: Stat. Mech. Appl. 286:321-336. https://doi.org/10.1016/S0378-4371(00)00335-6
  13. De Vos, P., Garrity, G. M., Jones, D., Krieg, N. R., Ludwig, W., Rainey, F. A., Schleifer, K.-H. and Whitman, W. B. 2009. Bergey's manual of systematic bacteriology. Vol. 3. The firmicutes. 2nd ed. Springer, New York, NY, USA. 1450 pp.
  14. Evans, T. A., Forschler, B. T. and Grace, J. K. 2013. Biology of invasive termites: a worldwide review. Annu. Rev. Entomol. 58:455-474. https://doi.org/10.1146/annurev-ento-120811-153554
  15. Gurung, K., Wertheim, B. and Salles, J. F. 2019. The microbiome of pest insects: it is not just bacteria. Entomol. Exp. Appl. 167:156-170. https://doi.org/10.1111/eea.12768
  16. Gkizi, D., Gonzalez Gil, A., Pardal, A. J., Piquerez, S., Sergaki, C., Ntoukakis, V. and Tjamos, S. E. 2021. The bacterial biocontrol agent Paenibacillus alvei K165 confers inherited resistance to Verticillium dahliae. J. Exp. Bot. 72:4565-4576. https://doi.org/10.1093/jxb/erab154
  17. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
  18. Hugh, R. and Leifson, E. 1953. The taxonomic significance of fermentative versus oxidative metabolism of carbohydrates by various gram negative bacteria. J. Bacteriol. 66:24-26. https://doi.org/10.1128/jb.66.1.24-26.1953
  19. Husseneder, C. 2010. Symbiosis in subterranean termites: a review of insights from molecular studies. Environ. Entomol. 39:378-388. https://doi.org/10.1603/EN09006
  20. Hyodo, F., Inoue, T., Azuma, J.-I., Tayasu, I. and Abe, T. 2000. Role of the mutualistic fungus in lignin degradation in the fungus-growing termite Macrotermes gilvus (Isoptera; Macrotermitinae). Soil Biol. Biochem. 32:653-658. https://doi.org/10.1016/S0038-0717(99)00192-3
  21. Ichielevich-Auster, M., Sneh, B., Koltin, Y. and Barash, I. 1985. Pathogenicity, host specificity and anastomosis groups of Rhizoctonia spp. isolated from soils in Israel. Phytoparasitica 13:103-112. https://doi.org/10.1007/BF02980887
  22. Jinal, H. N., Gopi, K., Prittesh, P., Kartik, V. P. and Amaresan, N. 2019. Phytoextraction of iron from contaminated soils by inoculation of iron-tolerant plant growth-promoting bacteria in Brassica juncea L. Czern. Environ. Sci. Pollut. Res. 26:32815-32823. https://doi.org/10.1007/s11356-019-06394-2
  23. Juan-abgona, R. V., Katsuno, N., Kageyama, K. and Hyakumachi, M. 1996. Isolation and identification of hypovirulent Rhizoctonia spp. from soil. Plant Pathol. 45:896-904. https://doi.org/10.1111/j.1365-3059.1996.tb02900.x
  24. Kalaiselvi, P., Jayashree, R. and Poornima, R. 2019. Plant growth promoting Bacillus spp. and Paenibacillus alvei on the growth of Sesuvium portulacastrum for phytoremediation of salt affected soils. Int. J. Curr. Microbiol. Appl. Sci. 8:2847-2858. https://doi.org/10.20546/ijcmas.2019.804.332
  25. Khayi, S., Cigna, J., Chong, T. M., Quetu-Laurent, A., Chan, K.-G., Helias, V. and Faure, D. 2016. Transfer of the potato plant isolates of Pectobacterium wasabiae to Pectobacterium parmentieri sp. nov. Int. J. Syst. Evol. Microbiol. 66:5379-5383. https://doi.org/10.1099/ijsem.0.001524
  26. Kim, H.-S., Ma, B., Perna, N. T. and Charkowski, A. O. 2009. Phylogeny and virulence of naturally occurring type III secretion system-deficient Pectobacterium strain. Appl. Environ. Microbiol. 75:4539-4549. https://doi.org/10.1128/AEM.01336-08
  27. Kumar, S., Stecher, G. and Tamura, K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33:1870-1874. https://doi.org/10.1093/molbev/msw054
  28. Lelliott, R. A., Billing, E. and Hayward, A. C. 1966. A determinative scheme for the fluorescent plant pathogenic pseudomonads. J. Appl. Bacteriol. 29:470-489. https://doi.org/10.1111/j.1365-2672.1966.tb03499.x
  29. Moleleki, L. N., Onkendi, E. M., Mongae, A. and Kubheka, G. C. 2013. Characterisation of pectobacterium wasabiae causing blackleg and soft rot diseases in South Africa. Eur. J. Plant Pathol. 135:279-288. https://doi.org/10.1007/s10658-012-0084-4
  30. Muniaraj, M., Dinesh, D. S., Sinha, P. K., Das, P. and Bhattacharya, S. K. 2008. Dual culture method to determine the relationship of gut bacteria of sandfly (Phlebotomus argentipes) with promastigotes of Leishmania donovani. J. Commun. Dis. 40:133-138.
  31. Nishiyama, K. 1978. The tentative plan of simple identification method of plant pathogenic bacteria. Shokubutsu Boeki 32:283-288.
  32. Park, M., Kim, C., Yang, J., Lee, H., Shin, W., Kim, S. and Sa, T. 2005. Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiol. Res. 160:127-133. https://doi.org/10.1016/j.micres.2004.10.003
  33. Passera, A., Rossato, M., Oliver, J. S., Battelli, G., Shahzad, G. I., Cosentino, E., Sage, J. M., Toffolatti, S. L., Lopatriello, G., Davis, J. R., Kaiser, M. D., Delledonne, M. and Casati, P. 2020. Characterization of Lysinibacillus fusiformis strain S4C11: In vitro, in planta, and in silico analyses reveal a plant-beneficial microbe. Microbiol. Res. 244:126665.
  34. Portier, P., Pedron, J., Taghouti, G., Fischer-Le Saux, M., Caullireau, E., Bertrand, C., Laurent, A., Chawki, K., Oulgazi, S., Moumni, M., Andrivon, D., Dutrieux, C., Faure, D., Helias, V. and Barny, M. A. 2019. Elevation of Pectobacterium carotovorum subsp. odoriferum to species level as Pectobacterium odoriferum sp. nov., proposal of Pectobacterium brasiliense sp. nov. and Pectobacterium actinidiae sp. nov., emended description of Pectobacterium carotovorum and description of Pectobacterium versatile sp. nov., isolated from streams and symptoms on diverse plants. Int. J. Syst. Evol. Microbiol. 69:3207-3216. https://doi.org/10.1099/ijsem.0.003611
  35. Ryu, E. 1940. A simple method of differentiation between grampositive and gram-negative organism without staining. Kitasato Arch. Exp. Med. 17:58-63.
  36. Schaad, N. W., Jones, J. B. and Chun, W. 2001. Laboratory guide for identification of plant pathogenic bacteria. 3rd ed. American Phytopathological Society Press, St. Paul, MN, USA. 373 pp.
  37. Sgroy, V., Cassan, F., Masciarelli, O., Del Papa, M. F., Lagares, A. and Luna, V. 2009. Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasisregulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl. Microbiol. Biotechnol. 85:371-381. https://doi.org/10.1007/s00253-009-2116-3
  38. Silhavy, T. J., Kahne, D. and Walker, S. 2010. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2:a000414.
  39. Singh, R. K., Kumar, D. P., Solanki, M. K., Singh, P., Srivastva, A. K., Kumar, S., Kashyap, P. L., Saxena, A. K., Singhal, P. K. and Arora, D. K. 2013. Optimization of media components for chitinase production by chickpea rhizosphere associated Lysinibacillus fusiformis B-CM18. J. Basic Microbiol. 53:451-460. https://doi.org/10.1002/jobm.201100590
  40. Skowronek, M., Sajnaga, E., Pleszczynska, M., Kazimierczak, W., Lis, M. and Wiater, A. 2020. Bacteria from the midgut of common cockchafer (Melolontha melolontha L.) larvae exhibiting antagonistic activity against bacterial symbionts of entomopathogenic nematodes: isolation and molecular identification. Int. J. Mol. Sci. 21:580.
  41. Sneh, B., Yamoah, E. and Stewart, A. 2004. Hypovirulent Rhizoctonia spp. isolates from New Zealand soils protect radish seedlings against damping-off caused by R. solani. N. Z. Plant Prot. 57:54-58.
  42. Suharjo, R., Aeny, T. N., Hasanudin, U., Sukmaratri T., Krisno, R., Khoironi, T. and Safitri, D. A. 2018. Potential of endophytic bacteria as plant growth promoter and antagonist against pineapple-fungal plant pathogen in Indonesia. In: Proceeding of International Symposium on Innovative Crop Protection for Sustainable Agriculture, pp. 41-44. The United Graduate School of Agricultural Science, Gifu University, Japan.
  43. Suharjo, R., Oktaviana, H. A., Aeny, T. N., Ginting, C., Wardhana, R. A., Nugroho, A. and Ratdiana, R. 2021. Erwinia mallotivora is the causal agent of papaya bacterial crown rot disease in Lampung Timur, Indonesia. Plant Prot. Sci. 57:122-133. https://doi.org/10.17221/123/2020-PPS
  44. Suharjo, R., Sawada, H. and Takikawa, Y. 2014. Phylogenetic study of Japanese Dickeya spp. and development of new rapid identification methods using PCR-RFLP. J. Gen. Plant Pathol. 80:230-254. https://doi.org/10.1007/s10327-014-0508-4
  45. Trakulnaleamsai, S., Hongoh, Y., Deevong, P. and Noparatnaraporn, N. 2004. Phylogenetic diversity of bacterial symbionts in the guts of wood-feeding termites. Kasetsart J. (Nat. Sci.). 38:45-51.
  46. Trivedi, P., Spann, T. and Wang, N. 2011. Isolation and characterization of beneficial bacteria associated with citrus roots in Florida. Microb. Ecol. 62:324-336. https://doi.org/10.1007/s00248-011-9822-y
  47. Weisburg, W. G., Barns, S. M., Pelletier, D. A. and Lane, D. J. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703. https://doi.org/10.1128/jb.173.2.697-703.1991