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International Journal of Microbiology
Volume 2018, Article ID 6280484, 13 pages
https://doi.org/10.1155/2018/6280484
Research Article

Bacterial Community of the Rice Floodwater Using Cultivation-Independent Approaches

1Programa de Pós-Graduação em Biologia, Universidade do Vale do Rio dos Sinos (UNISINOS), 950 Unisinos Avenue, São Leopoldo, RS, Brazil
2United States Department of Agriculture (USDA), Agricultural Research Service (ARS), Center for Grain and Animal Health Research, Stored Product Insect and Engineering Research Unit (SPIERU), 1515 College Ave., Manhattan, KS, USA
3United States Department of Agriculture (USDA), Agricultural Research Service (ARS), Agroecosystem Management Research Unit (AMRU), 251 Filley Hall, UNL East Campus, Lincoln, NE, USA

Correspondence should be addressed to Michele Pittol; moc.liamg@llottipim

Received 2 August 2017; Revised 9 December 2017; Accepted 26 December 2017; Published 30 January 2018

Academic Editor: Clemencia Chaves-López

Copyright © 2018 Michele Pittol et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. IRRI - International Rice Research Institute, “Rice in America Latine, past, present, and promising future,” Rice Today, vol. 14, pp. 1–23, 2015. View at Google Scholar
  2. GRiSP - Global Rice Science Partnership, “Rice almanac,” Los Baños, Philippines: International Rice Research Institute, 2012.
  3. T. Shibagaki-Shimizu, N. Nakayama, Y. Nakajima, K. Matsuya, M. Kimura, and S. Asakawa, “Phylogenetic study on a bacterial community in the floodwater of a Japanese paddy field estimated by sequencing 16S rDNA fragments after denaturing gradient gel electrophoresis,” Biology and Fertility of Soils, vol. 42, no. 4, pp. 362–365, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. A. E. Bernhard, D. Colbert, J. McManus, and K. G. Field, “Microbial community dynamics based on 16S rRNA gene profiles in a Pacific Northwest estuary and its tributaries,” FEMS Microbiology Ecology, vol. 52, no. 1, pp. 115–128, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. A. R. Lopes, C. M. Manaia, and O. C. Nunes, “Bacterial community variations in an alfalfa-rice rotation system revealed by 16S rRNA gene 454-pyrosequencing,” FEMS Microbiology Ecology, vol. 87, no. 3, pp. 650–663, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Zhao, T. Ni, W. Xun et al., “Influence of straw incorporation with and without straw decomposer on soil bacterial community structure and function in a rice-wheat cropping system,” Applied Microbiology and Biotechnology, vol. 101, no. 11, pp. 4761–4773, 2017. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Breidenbach and R. Conrad, “Seasonal dynamics of bacterial and archaeal methanogenic communities in flooded rice fields and effect of drainage,” Frontiers in Microbiology, vol. 5, article 752, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. B. Breidenbach, M. B. Blaser, M. Klose, and R. Conrad, “Crop rotation of flooded rice with upland maize impacts the resident and active methanogenic microbial community,” Environmental Microbiology, vol. 18, no. 9, pp. 2868–2885, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. D. E. Koeck, A. Pechtl, V. V. Zverlov, and W. H. Schwarz, “Genomics of cellulolytic bacteria,” Current Opinion in Biotechnology, vol. 29, pp. 171–183, 2014. View at Publisher · View at Google Scholar
  10. H. Itoh, S. Ishii, Y. Shiratori et al., “Seasonal transition of active bacterial and archaeal communities in relation to water management in paddy soils,” Microbes and Environments, vol. 28, no. 3, pp. 370–380, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. Y.-J. Li, X. Chen, I. H. Shamsi, P. Fang, and X.-Y. Lin, “Effects of Irrigation Patterns and Nitrogen Fertilization on Rice Yield and Microbial Community Structure in Paddy Soil,” Pedosphere, vol. 22, no. 5, pp. 661–672, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. I. Loaces, L. Ferrando, and A. F. Scavino, “Dynamics, Diversity and Function of Endophytic Siderophore-Producing Bacteria in Rice,” Microbial Ecology, vol. 61, no. 3, pp. 606–618, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Prakamhang, K. Minamisawa, K. Teamtaisong, N. Boonkerd, and N. Teaumroong, “The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L.),” Applied Soil Ecology, vol. 42, no. 2, pp. 141–149, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. R. de Souza, A. Beneduzi, A. Ambrosini et al., “The effect of plant growth-promoting rhizobacteria on the growth of rice (Oryza sativa L.) cropped in southern Brazilian fields,” Plant and Soil, vol. 366, no. 1-2, pp. 585–603, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. A. F. Scavino, J. Menes, L. Ferrando, and S. Tarlera, “Bacterial community analysis of the water surface layer from a rice-planted and an unplanted flooded field,” Brazilian Journal of Microbiology, vol. 41, no. 2, pp. 411–419, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. W. Mhuantong, S. Wongwilaiwalin, T. Laothanachareon et al., “Survey of microbial diversity in flood areas during Thailand 2011 flood crisis using high-throughput tagged amplicon pyrosequencing,” PLoS ONE, vol. 10, no. 5, Article ID e0128043, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. P. A. Counce, T. C. Keisling, and A. J. Mitchell, “A uniform, objectives, and adaptive system for expressing rice development,” Crop Science, vol. 40, no. 2, pp. 436–443, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. A. D. Eaton, L. S. Clesceri, A. E. Greenberg, and M. A. H. Franson, Standard Methods for the Examination of Water and Wastewater, APHA-AWWA-WPCF, Washington, DC, USA, 1998.
  19. J. G. Caporaso, C. L. Lauber, W. A. Walters et al., “Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 108, no. 1, pp. 4516–4522, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. M. J. Tedesco, C. Gianello, C. A. Bissani, H. Bohnen, and S. J. Volkweiss, Análise de Solo, Plantas e Outros Materiais, Departamento de Solos da Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil, 1995.
  21. L. Bortolon and C. Gianello, “Simultaneous multielement extraction with the mehlich-1 solution for southern Brazilian soils determined by ICP-OES and the effects on the nutrients recommendations to crops,” Revista Brasileira de Ciência do Solo, vol. 34, no. 1, pp. 125–132, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. P. D. Schloss, S. L. Westcott, T. Ryabin et al., “Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities,” Applied and Environmental Microbiology, vol. 75, no. 23, pp. 7537–7541, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Quince, A. Lanzén, T. P. Curtis et al., “Accurate determination of microbial diversity from 454 pyrosequencing data,” Nature Methods, vol. 6, no. 9, pp. 639–641, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. “Silva reference files (release 123),” http://www.mothur.org/wiki/Silva_reference_files, 2017.
  25. R. C. Edgar, B. J. Haas, J. C. Clemente, C. Quince, and R. Knight, “UCHIME improves sensitivity and speed of chimera detection,” Bioinformatics, vol. 27, no. 16, pp. 2194–2200, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Chao, R. L. Chazdon, and T. J. Shen, “A new statistical approach for assessing similarity of species composition with incidence and abundance data,” Ecology Letters, vol. 8, no. 2, pp. 148–159, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Oksanen, R. Kindt, P. Legendre, B. O'Hara, and M. H. H. Stevens, “The vegan package,” https://r-forge.r-project.org/projects/vegan/, 2007.
  28. M. Diel, R. M. V. Castilhos, R. O. De Sousa, L. C. Valh, and J. B. Da Silva, “Nutrients in the water for irrigation of rice in the South region of the State of Rio Grande do Sul, Brazil,” Ciência Rural, vol. 37, no. 1, pp. 102–109, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. S. L. Machado, E. Marchezan, A. A. Righes, R. Carlesso, S. C. Villa, and E. R. Camargo, “Consumo de água e perdas de nutrientes e de sedimentos na água de drenagem inicial do arroz irrigado,” Ciência Rural, vol. 36, no. 1, pp. 65–71, 2006. View at Publisher · View at Google Scholar
  30. D. Alongi, “The role of bacteria in nutrient recycling in tropical mangrove and other coastal benthic ecosystems,” in Ecology and Conservation of Southeast Asian Marine and Freshwater Environments Including Wetlands. Developments in Hydrobiology, A. Sasekumar, N. Marshall, and D. J. Macintosh, Eds., pp. 19–32, Springer, Dordrecht, Netherlands, 1994. View at Google Scholar
  31. A. Okabe, K. Toyota, and M. Kimura, “Seasonal variations of phospholipid fatty acid composition in the floodwater of a japanese paddy field under a long-term fertilizer trial,” Soil Science & Plant Nutrition, vol. 46, no. 1, pp. 177–188, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Barreiros, C. M. Manaia, and O. C. Nunes, “Bacterial diversity and bioaugmentation in floodwater of a paddy field in the presence of the herbicide molinate,” Biodegradation, vol. 22, no. 2, pp. 445–461, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Nakayama, A. Okabe, K. Toyota, M. Kimura, and S. Asakawa, “Phylogenetic distribution of bacteria isolated from the floodwater of a Japanese paddy field,” Soil Science & Plant Nutrition, vol. 52, no. 3, pp. 305–312, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Lu, A. Watanabe, and M. Kimura, “Contribution of plant-derived carbon to soil microbial biomass dynamics in a paddy rice microcosm,” Biology and Fertility of Soils, vol. 36, no. 2, pp. 136–142, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. Q. Hussain, G. X. Pan, Y. Z. Liu et al., “Microbial community dynamics and function associated with rhizosphere over periods of rice growth,” Plant, Soil and Environment, vol. 58, pp. 55–61, 2012. View at Google Scholar
  36. H. J. Lee, S. Y. Kim, P. J. Kim, E. L. Madsen, and C. O. Jeon, “Methane emission and dynamics of methanotrophic and methanogenic communities in a flooded rice field ecosystem,” FEMS Microbiology Ecology, vol. 88, no. 1, pp. 195–212, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Fernández-Valiente and A. Quesada, “A shallow water ecosystem: Rice-fields. The relevance of cyanobacteria in the ecosystem,” Limnetica, vol. 23, no. 1-2, pp. 95–108, 2004. View at Google Scholar · View at Scopus
  38. Y. Wang, H. F. Sheng, Y. He et al., “Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags,” Applied and Environmental Microbiology, vol. 78, no. 23, pp. 8264–8271, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Asakawa and M. Kimura, “Comparison of bacterial community structures at main habitats in paddy field ecosystem based on DGGE analysis,” Soil Biology & Biochemistry, vol. 40, no. 6, pp. 1322–1329, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Ren, H. Zhang, X. Lin, J. Zhu, and Z. Jia, “Response of phyllosphere bacterial communities to elevated CO2 during rice growing season,” Applied Microbiology and Biotechnology, vol. 98, no. 22, pp. 9459–9471, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. M. S. Aulakh, R. Wassmann, C. Bueno, J. Kreuzwieser, and H. Rennenberg, “Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars,” The Journal of Plant Biology, vol. 3, no. 2, pp. 139–148, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. B. Lugtenberg and F. Kamilova, “Plant-growth-promoting rhizobacteria,” Annual Review of Microbiology, vol. 63, pp. 541–556, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. D. L. Jones, A. Hodge, and Y. Kuzyakov, “Plant and mycorrhizal regulation of rhizodeposition,” New Phytologist, vol. 163, no. 3, pp. 459–480, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Gupta, J. Panwar, M. S. Akhtar, and P. N. Jha, “Endophytic Nitrogen-Fixing Bacteria as Biofertilizer,” Sustainable Agriculture Reviews, vol. 11, pp. 183–221, 2012. View at Publisher · View at Google Scholar
  45. H. P. Bais, T. L. Weir, L. G. Perry, S. Gilroy, and J. M. Vivanco, “The role of root exudates in rhizosphere interactions with plants and other organisms,” Annual Review of Plant Biology, vol. 57, no. 1, pp. 233–266, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Ziegler, M. Engel, G. Welzl, and M. Schloter, “Development of a simple root model to study the effects of single exudates on the development of bacterial community structure,” Journal of Microbiological Methods, vol. 94, no. 1, pp. 30–36, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. A. P. King, K. J. Evatt, J. Six, R. M. Poch, D. E. Rolston, and J. W. Hopmans, “Annual carbon and nitrogen loadings for a furrow-irrigated field,” Agricultural Water Management, vol. 96, no. 6, pp. 925–930, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. A. Vorholt, “Microbial life in the phyllosphere,” Nature Reviews Microbiology, vol. 10, no. 12, pp. 828–840, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. J. B. Chiaramonte, M. D. C. Roberto, and T. A. Pagioro, “Seasonal dynamics and community structure of bacterioplankton in upper Paraná River floodplain,” Microbial Ecology, vol. 66, no. 4, pp. 773–783, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. R. J. Newton and K. D. Mcmahon, “Seasonal differences in bacterial community composition following nutrient additions in a eutrophic lake,” Environmental Microbiology, vol. 13, no. 4, pp. 887–899, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. A. C. Poot-Hernandez, K. Rodriguez-Vazquez, and E. Perez-Rueda, “The alignment of enzymatic steps reveals similar metabolic pathways and probable recruitment events in Gammaproteobacteria,” BMC Genomics, vol. 16, no. 1, article 957, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Ofek, Y. Hadar, and D. Minz, “Ecology of root colonizing Massilia (Oxalobacteraceae),” PLoS ONE, vol. 7, no. 7, Article ID e40117, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. D. S. Thuler, E. I. S. Floh, W. Handro, and H. R. Barbosa, “Plant growth regulators and amino acids released by Azospirillum sp. in chemically defined media,” Letters in Applied Microbiology, vol. 37, no. 2, pp. 174–178, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. J. A. Chapman, E. F. Kirkness, O. Simakov et al., “The dynamic genome of Hydra,” Nature, vol. 464, pp. 592–596, 2010. View at Google Scholar
  55. G. Zwart, B. C. Crump, M. P. Kamst-van Agterveld, F. Hagen, and S.-K. Han, “Typical freshwater bacteria: An analysis of available 16S rRNA gene sequences from plankton of lakes and rivers,” Aquatic Microbial Ecology, vol. 28, no. 2, pp. 141–155, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Hougardy and J.-H. Klemme, “Nitrate reduction in a new strain of Rhodoferax fermentans,” Archives of Microbiology, vol. 164, no. 5, pp. 358–362, 1995. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Terakado-Tonooka, Y. Ohwaki, H. Yamakawa, F. Tanaka, T. Yoneyama, and S. Fujihara, “Expressed nifH genes of endophytic bacteria detected in field-grown sweet potatoes (Ipomoea batatas L.),” Microbes and Environments, vol. 23, no. 1, pp. 89–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Crevecoeur, W. F. Vincent, J. Comte, and C. Lovejoy, “Bacterial community structure across environmental gradients in permafrost thaw ponds: Methanotroph-rich ecosystems,” Frontiers in Microbiology, vol. 6, article 192, 2015. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Jezbera, J. Jezberová, U. Brandt, and M. W. Hahn, “Ubiquity of Polynucleobacter necessarius subspecies asymbioticus results from ecological diversification,” Environmental Microbiology, vol. 13, no. 4, pp. 922–931, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Horňák, V. Kasalický, K. Šimek, and H. Grossart, “Strain-specific consumption and transformation of alga-derived dissolved organic matter by members of the,” Environmental Microbiology, vol. 19, no. 11, pp. 4519–4535, 2017. View at Publisher · View at Google Scholar
  61. M. W. Hahn, T. Scheuerl, J. Jezberová et al., “The passive yet successful way of planktonic life: Genomic and experimental analysis of the ecology of a free-living polynucleobacter population,” PLoS ONE, vol. 7, no. 3, Article ID e32772, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. D. T. A. Tuyet, T. Tanaka, R. Sohrin, D. M. Hao, K. Nagaosa, and K. Kato, “Effects of warming on microbial communities in the coastal waters of temperate and subtropical zones in the Northern Hemisphere, with a focus on Gammaproteobacteria,” Journal of Oceanography, vol. 71, no. 1, pp. 91–103, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Reim, M. Hernández, M. Klose, A. Chidthaisong, M. Yuttitham, and R. Conrad, “Response of methanogenic microbial communities to desiccation stress in flooded and rain-fed paddy soil from Thailand,” Frontiers in Microbiology, vol. 8, no. MAY, article 785, 2017. View at Publisher · View at Google Scholar · View at Scopus
  64. J. Rui, J. Peng, and Y. Lu, “Succession of bacterial populations during plant residue decomposition in rice field soil,” Applied and Environmental Microbiology, vol. 75, no. 14, pp. 4879–4886, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Kim and W. Liesack, “Differential assemblage of functional units in paddy soil microbiomes,” PLoS ONE, vol. 10, no. 4, Article ID e0122221, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. J. Tian, M. Dippold, J. Pausch et al., “Microbial response to rhizodeposition depending on water regimes in paddy soils,” Soil Biology & Biochemistry, vol. 65, pp. 195–203, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Mougel, P. Offre, L. Ranjard et al., “Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5,” New Phytologist, vol. 170, no. 1, pp. 165–175, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. W. X. Wu, W. Liu, H. H. Lu, Y. X. Chen, M. Devare, and J. Thies, “Use of 13C labeling to assess carbon partitioning in transgenic and nontransgenic (parental) rice and their rhizosphere soil microbial communities,” FEMS Microbiology Ecology, vol. 67, no. 1, pp. 93–102, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Zancarini, C. Lépinay, J. Burstin et al., “Combining Molecular Microbial Ecology with Ecophysiology and Plant Genetics for a Better Understanding of Plant-Microbial Communities' Interactions in the Rhizosphere,” in Molecular Microbial Ecology of the Rhizosphere, F. J. D. Bruijn, Ed., vol. 1, pp. 69–86, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. M. H. L. R. Reche and L. M. Fiuza, “Bacterial diversity in rice-field water in Rio Grande do Sul,” Brazilian Journal of Microbiology, vol. 36, no. 3, pp. 253–257, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. J. P. Panizzon, V. R. M. MacEdo, V. MacHado, and L. M. Fiuza, “Microbiological and physical-chemical water quality of the rice fields in Sinos River's basin, Southern Brazil,” Environmental Modeling & Assessment, vol. 185, no. 3, pp. 2767–2775, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. T. Ge, H. Yuan, H. Zhu et al., “Biological carbon assimilation and dynamics in a flooded rice-soil system,” Soil Biology & Biochemistry, vol. 48, pp. 39–46, 2012. View at Publisher · View at Google Scholar
  73. N. Fierer, C. L. Lauber, K. S. Ramirez, J. Zaneveld, M. A. Bradford, and R. Knight, “Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients,” The ISME Journal, vol. 6, no. 5, pp. 1007–1017, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. S. K. Dubey and J. S. Singh, “Spatio-temporal variation and effect of urea fertilization on methanotrophs in a tropical dryland rice field,” Soil Biology & Biochemistry, vol. 32, no. 4, pp. 521–526, 2000. View at Publisher · View at Google Scholar · View at Scopus