Enrichment of bacteria involved in the nitrogen cycle and plant growth promotion in soil by sclerotia of rice sheath blight fungus

Mirza Abid Mehmood, Yanping Fu, Huizhang Zhao, Jiasen Cheng, Jiatao Xie, Daohong Jiang

Stress Biology ›› 2022, Vol. 2 ›› Issue (1) : 32. DOI: 10.1007/s44154-022-00049-y
Original Paper

Enrichment of bacteria involved in the nitrogen cycle and plant growth promotion in soil by sclerotia of rice sheath blight fungus

Author information +
History +

Abstract

Rice sheath blight pathogen, Rhizoctonia solani, produces numerous sclerotia to overwinter. As a rich source of nutrients in the soil, sclerotia may lead to the change of soil microbiota. For this purpose, we amended the sclerotia of R. solani in soil and analyzed the changes in bacterial microbiota within the soil at different time points. At the phyla level, Proteobacteria, Acidobacteria, Bacteroidetes, Actinobacteria, Chloroflexi and Firmicutes showed varied abundance in the amended soil samples compared to those in the control. An increased abundance of ammonia-oxidizing bacterium (AOB) Nitrosospira and Nitrite oxidizing bacteria (NOB) i.e., Nitrospira was observed, where the latter is reportedly involved in the nitrifier denitrification. Moreover, Thiobacillus, Gemmatimonas, Anaeromyxobacter and Geobacter, the vital players in denitrification, N2O reduction and reductive nitrogen transformation, respectively, depicted enhanced abundance in R. solani sclerotia-amended samples. Furthermore, asymbiotic nitrogen-fixing bacteria, notably, Azotobacter as well as Microvirga and Phenylobacterium with nitrogen-fixing potential also enriched in the amended samples compared to the control. Plant growth promoting bacteria, such as Kribbella, Chitinophaga and Flavisolibacter also enriched in the sclerotia-amended soil. As per our knowledge, this study is of its kind where pathogenic fungal sclerotia activated microbes with a potential role in N transformation and provided clues about the ecological functions of Rsolani sclerotia on the stimulation of bacterial genera involved in different processes of N-cycle within the soil in the absence of host plants.

Keywords

Rice sheath blight / Rhizoctonia solani / Sclerotia / Reductive nitrogen transformation / Nitrogen fixation / Soil microbiome

Cite this article

Download citation ▾
Mirza Abid Mehmood, Yanping Fu, Huizhang Zhao, Jiasen Cheng, Jiatao Xie, Daohong Jiang. Enrichment of bacteria involved in the nitrogen cycle and plant growth promotion in soil by sclerotia of rice sheath blight fungus. Stress Biology, 2022, 2(1): 32 https://doi.org/10.1007/s44154-022-00049-y

References

[1]
AnandhamR, GandhiPI, MadhaiyanM, SaT. Potential plant growth promoting traits and bioacidulation of rock phosphate by thiosulfate oxidizing bacteria isolated from crop plants. J Basic Microbiol, 2008, 48: 439-447
CrossRef Google scholar
[2]
AndersonMJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol, 2001, 26: 32-46
CrossRef Google scholar
[3]
BachEM, WilliamsRJ, HargreavesSK, YangF, HofmockelKS. Greatest soil microbial diversity found in micro-habitats. Soil Biol Biochem, 2018, 118: 217-226
CrossRef Google scholar
[4]
Beckers B, Op De Beeck M, Thijs S, Truyens S, Weyens N, Boerjan W, Vangronsveld J (2016) Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies. Front Microbiol 7:650. https://doi.org/10.3389/fmicb.2016.00650
[5]
BokulichNA, SubramanianS, FaithJJ, GeversD, GordonJI, KnightR, MillsDA, CaporasoJG. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods, 2013, 10: 57-59
CrossRef Google scholar
[6]
CaporasoJG, LauberCL, WaltersWA, Berg-LyonsD, LozuponeCA, TurnbaughPJ, FiererN, KnightR. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci, 2011, 108: 4516-4522
CrossRef Google scholar
[7]
ChenZ, LiuJ, WuM, XieX, WuJ, WeiW. Differentiated response of denitrifying communities to fertilization regime in paddy soil. Microb Ecol, 2012, 63: 446-459
CrossRef Google scholar
[8]
ColliverBB, StephensonT. Production of nitrogen oxide and dinitrogen oxide by autotrophic nitrifiers. Biotechnol Adv, 2000, 18: 219-232
CrossRef Google scholar
[9]
CuRM, MewTW, CassmanKG, TengPS. Effect of sheath blight in tropical, intensive rice production system. Plant Dis, 1996, 80: 1103-1108
CrossRef Google scholar
[10]
da SilveiraJAG, Da CostaRCL, OliveiraJTA. Drought-induced effects and recovery of nitrate assimilation and nodule activity in cowpea plants inoculated with Bradyrhizobium spp. under moderate nitrate level. Brazilian J Microbiol, 2001, 32: 187-194
CrossRef Google scholar
[11]
De Ca´ceres M, Legendre P,. Associations between species and groups of sites: indices and statistical inference. Ecology, 2009, 90: 3566-3574
CrossRef Google scholar
[12]
DemanècheS, PhilippotL, DavidMM, NavarroE, VogelTM, SimonetP. Characterization of denitrification gene clusters of soil bacteria via a metagenomic approach. Appl Environ Microbiol, 2009, 75: 534-537
CrossRef Google scholar
[13]
DingLJ, SuJQ, XuHJ, JiaZJ, ZhuYG. Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-13C-acetate probing coupled with pyrosequencing. ISME J, 2015, 9: 721-734
CrossRef Google scholar
[14]
DixonR, KahnD. Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol, 2004, 2: 621-631
CrossRef Google scholar
[15]
EdgarRC, HaasBJ, ClementeJC, QuinceC, KnightR. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 2011, 27: 2194-2200
CrossRef Google scholar
[16]
Esitken A, Ercisli S, Karlidag H, Sahin F (2005) Potential use of plant growth promoting rhizobacteria (PGPR) in organic apricot production. Libek A,Kaufmane E, Sasnauskas A, editors. Proceedings of the International ScientificConference of Environmentally Friendly Fruit Growing. pp. 90–97
[17]
FAO (2004). Rice is Life. FAO, Italy. http://www.fao.org/newsroom/en/focus/2004/36887/index.html. Accessed 2 Apr 2018
[18]
[19]
FengS, ShuC, WangC, JiangS, ZhouE. Survival of Rhizoctonia solani AG-1 IA, the causal agent of rice sheath blight, under different environmental conditions. J Phytopathol, 2017, 165: 44-52
CrossRef Google scholar
[20]
FiererN, BradfordMA, JacksonRB. Toward an ecological classification of soil bacteria. Ecology, 2007, 88: 1354-1364
CrossRef Google scholar
[21]
FrancheC, LindströmK, ElmerichC. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil, 2009, 321: 35-59
CrossRef Google scholar
[22]
Freitas SS (2007) Rizobactérias promotoras de crescimento de plantas. In: Silveira APD, Freitas SS (eds) Microbiota do solo e qualidade ambiental. Instituto Agronômico de Campinas, Campinas, pp 1–20
[23]
FujitaniH, AoiY, TsunedaS. Selective enrichment of two different types of Nitrospira-like nitrite-oxidizing bacteria from a wastewater treatment plant. Microbes Environ, 2013, 28: 236-243
CrossRef Google scholar
[24]
González-VeraAD, Bernardes-De-AssisJ, ZalaM, McDonaldBA, Correa-VictoriaF, Graterol-MatuteEJ, CeresiniPC. Divergence between sympatric rice-and maize-infecting populations of Rhizoctonia solani AG-1 IA from Latin America. Phytopathol, 2010, 100: 172-182
CrossRef Google scholar
[25]
GottelNR, CastroHF, KerleyM, YangZM, PelletierDA, PodarM, KarpinetsT, UberbacherE, TuskanGA, VilgalysR, DoktyczMJ, SchadtCW. Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol, 2011, 77: 5934-5944
CrossRef Google scholar
[26]
GrossE, CordeiroL, CaetanoFH. Nodulação e micorrização Anadenanthera peregrina var. falcata em solo de cerrado autoclavado e não autoclavado. Rev Bras Cienc Do Solo, 2004, 28: 95-101
CrossRef Google scholar
[27]
HaasBJ, GeversD, EarlAM, FeldgardenM, WardDV, GiannoukosG, CiullaD, TabbaaD, HighlanderSK, SodergrenE, MetheB, DeSantisTZ, PetrosinoJF, KnightR, BirrenBW. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res, 2011, 21: 494-504
CrossRef Google scholar
[28]
HoultonBZ, BaiE. Imprint of denitrifying bacteria on the global terrestrial biosphere. Proc Natl Acad Sci U S A, 2009, 106: 21713-21716
CrossRef Google scholar
[29]
HuseSM, WelchDM, MorrisonHG, SoginML. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol, 2010, 12: 1889-1898
CrossRef Google scholar
[30]
Igarashi M, Sawa R, Yamasaki M, Hayashi C, Umekita M, Hatano M, Fujiwara T, Mizumoto K, Nomoto A (2017) Kribellosides, novel RNA 5′-triphosphatase inhibitors from the rare actinomycete Kribbella sp. MI481-42F6. J Antibiot (tokyo) 70:582–589. https://doi.org/10.1038/ja.2016.161
[31]
Inaba S, Ikenishi F, Itakura M, Kikuchi M, Eda S, Chiba N, Katsuyama C, Suwa Y, Mitsui H, Minamisawa K (2012) N2O emission from degraded soybean nodules depends on denitrification by Bradyrhizobium japonicum and other microbes in the rhizosphere. Microbes Environ 27:470–476. https://doi.org/10.1264/jsme2.me12100
[32]
IshiiS, IkedaS, MinamisawaK, SenooK. Nitrogen cycling in rice paddy environments: Past achievements and future challenges. Microbes Environ, 2011, 26: 282-292
CrossRef Google scholar
[33]
Jaiswal AK, Elad Y, Paudel I, Graber ER, Cytryn E, Frenkel O (2017) Linking the belowground microbial composition, diversity and activity to soilborne disease suppression and growth promotion of tomato amended with biochar. Sci Rep 7:44382. https://doi.org/10.1038/srep44382
[34]
KaurK, GoyalS, KapoorKK. Impact of organic fertilizers with and without chemical fertilizers on soil chemical properties and the establishment of nitrogen-fixing bacteria in the rhizosphere. Microbes Environ, 2008, 23: 313-316
CrossRef Google scholar
[35]
KimY, LiesackW. Differential assemblage of functional units in paddy soil microbiomes. PLoS ONE, 2015, 10: 1-20
CrossRef Google scholar
[36]
KoldeR. pheatmap: Pretty Heatmaps. R Package Version, 2015, 1: 8
[37]
KondoK, YoshimatsuK, FujiwaraT. Expression, and molecular and enzymatic characterization of Cu-containing nitrite reductase from a marine ammonia-oxidizing gammaproteobacterium, Nitrosococcus oceani. Microbes Environ, 2012, 27: 407-412
CrossRef Google scholar
[38]
KongBH, TanNH, FungSY, PailoorJ, TanCS, NgST. Nutritional composition, antioxidant properties, and toxicology evaluation of the sclerotium of Tiger Milk Mushroom Lignosus tigris cultivar E. Nutr Res, 2016, 36: 174-183
CrossRef Google scholar
[39]
KozichJJ, WestcottSL, BaxterNT, HighlanderSK, SchlossPD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Appl Environ Microbiol, 2013, 79: 5112-5120
CrossRef Google scholar
[40]
LeeF. Number, viability, and buoyancy of Rhizoctonia solani sclerotia in Arkansas rice fields. Plant Dis, 1980, 64: 298-300
CrossRef Google scholar
[41]
LienhardP, TerratS, Prévost-BouréNC, NowakV, RegnierT, SayphoummieS, PanyasiriK, TivetF, MathieuO, LevequeJ, MaronPA, RanjardL. Pyrosequencing evidences the impact of cropping on soil bacterial and fungal diversity in Laos tropical grassland. Agron Sustain Dev, 2014, 34: 525-533
CrossRef Google scholar
[42]
LinS, IqbalJ, HuR, ShaabanM, CaiJ, ChenX. Nitrous oxide emissions from yellow brown soil as affected by incorporation of crop residues with different carbon-to-nitrogen ratios: A case study in central China. Arch Environ Contam Toxicol, 2013, 65: 183-192
CrossRef Google scholar
[43]
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. https://doi.org/10.14806/ej.17.1.200
[44]
MasudaY, ItohH, ShiratoriY, IsobeK, OtsukaS, SenooK. Predominant but previously-overlooked prokaryotic drivers of reductive nitrogen transformation in paddy soils, revealed by metatranscriptomics. Microbes Environ, 2017, 32: 180-183
CrossRef Google scholar
[45]
Mehmood MA, Zhao H, Cheng J, Xie J, Jiang D, Fu Y (2020) Sclerotia of a phytopathogenic fungus restrict microbial diversity and improve soil health by suppressing other pathogens and enriching beneficial microorganisms. J Environ Manage 259:109857. https://doi.org/10.1016/j.jenvman.2019.109857
[46]
MollaKA, KarmakarS, MollaJ, BajajP, VarshneyRK, DattaSK, DattaK. Understanding sheath blight resistance in rice: the road behind and the road ahead. Plant Biotechnol J, 2020, 18: 895-915
CrossRef Google scholar
[47]
Newton WE (2000) Nitrogen fixation in perspective. In: Pedrosa FO, Hungria M, Yates MG, Newton WE (eds) Nitrogen Fixation: From Molecules to Crop Productivity. Kluwer Academic Publishers, Dordrecht, pp 3–8. https://doi.org/10.1007/0-306-47615-0_1
[48]
OkuboT, TsukuiT, MaitaH, et al.. Complete genome sequence of Bradyrhizobium sp. S23321: Insights into symbiosis evolution in soil oligotrophs. Microbes Environ, 2012, 27: 306-315
CrossRef Google scholar
[49]
PalaniappanP, ChauhanPS, SaravananVS, AnandhamR, SaT. Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fertil Soils, 2010, 46: 807-816
CrossRef Google scholar
[50]
ParejaL, Fernández-AlbaAR, CesioV, HeinzenH. Analytical methods for pesticide residues in rice. TrAC - Trends Anal Chem, 2011, 30: 270-291
CrossRef Google scholar
[51]
Park D, Kim H, Yoon S (2017) Nitrous oxide reduction by an obligate aerobic bacterium, Gemmatimonas aurantiaca strain T-27. Appl Environ Microbiol 83:e00502-e517. https://doi.org/10.1128/AEM.00502-17
[52]
PhilippotL, HallinS, SchloterM. Ecology of denitrifying prokaryotes in agricultural soil. Adv Agron, 2007, 96: 249-305
CrossRef Google scholar
[53]
PielouEC. The measurement of diversity in different types of biological collections. J Theor Biol, 1966, 13: 131-144
CrossRef Google scholar
[54]
RadlV, Simões-AraújoJL, LeiteJ, PassosSR, MartinsLMV, XavierGR, RumjanekNG, BaldaniJI, ZilliJE. Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. Int J Syst Evol Microbiol, 2014, 64: 725-730
CrossRef Google scholar
[55]
Rao TB, Chopperla R, Prathi NB, Balakrishnan M, Prakasam V, Laha GS, Balachandran SM, Mangrauthia SK (2020) A comprehensive gene expression profile of pectin degradation enzymes reveals the molecular events during cell wall degradation and pathogenesis of rice sheath blight pathogen Rhizoctonia solani AG1-IA. J Fungi 6(2):71. https://doi.org/10.3390/jof6020071
[56]
RöschC, MergelA, BotheH. Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl Environ Microbiol, 2002, 68: 3818-3829
CrossRef Google scholar
[57]
SaitoI. Ultrastructural aspects of the maturation of sclerotia of Sclerotinia sclerotiorum (Lib.) de Bary. Trans Mycol Soc Japan, 1974, 15: 384-400
[58]
Schloss PD (2009) A high-throughput DNA sequence aligner for microbial ecology studies. PLoS ONE 4:e8230. https://doi.org/10.1371/journal.pone.0008230
[59]
Schloss PD (2010) The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput Biol 6:e1000844. https://doi.org/10.1371/journal.pcbi.1000844
[60]
SchlossPD. Secondary structure improves OTU assignments of 16S rRNA gene sequences. ISME J, 2013, 7: 457-460
CrossRef Google scholar
[61]
SchlossPD, WestcottSL. Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol, 2011, 77: 3219-3226
CrossRef Google scholar
[62]
SchlossPD, WestcottSL, RyabinT, et al.. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol, 2009, 75: 7537-7541
CrossRef Google scholar
[63]
ShawLJ, NicolGW, SmithZ, FearJ, ProsserJI, BaggsEM. Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol, 2006, 8: 214-222
CrossRef Google scholar
[64]
ShresthaCL, OñaI, MuthukrishnanS, MewTW. Chitinase levels in rice cultivars correlate with resistance to the sheath blight pathogen Rhizoctonia solani. Eur J Plant Pathol, 2007, 120: 69-77
CrossRef Google scholar
[65]
SmitE, LeeflangP, GommansS, Van Den BroekJ, Van MilS, WernarsK. Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol, 2001, 67: 2284-2291
CrossRef Google scholar
[66]
SteinbeissS, BeblerH, EngelsC, TempertonVM, BuchmannN, RoscherC, KreutzigerY, BaadeJ, HabekostM, GleixnerG. Plant diversity positively affects short-term soil carbon storage in experimental grasslands. Glob Chang Biol, 2008, 14: 2937-2949
CrossRef Google scholar
[67]
StrapJL. MaheshwariKD. Actinobacteria–plant interactions: a boon to agriculture. In Bacteria in Agrobiology: Plant Growth Responses, 2011 Berlin Springer
[68]
SunX, LiuD, WangY, MaA. Biogenesis of macrofungal sclerotia: influencing factors and molecular mechanisms. Appl Microbiol Biotechnol, 2020, 104: 4227-4234
CrossRef Google scholar
[69]
TaheriP, TarighiS. Cytomolecular aspects of rice sheath blight caused by Rhizoctonia solani. Eur J Plant Pathol, 2011, 129: 511-528
CrossRef Google scholar
[70]
Team RDC. R: A Language And Environment For Statistical Computing, 2017 Vienna, Austria R Foundation for Statistical Computing
[71]
ThamdrupB. New pathways and processes in the global nitrogen cycle. Annu Rev Ecol Evol Syst, 2012, 43: 407-428
CrossRef Google scholar
[72]
UekiT, LovleyDR. Novel regulatory cascades controlling expression of nitrogen-fixation genes in Geobacter sulfurreducens. Nucleic Acids Res, 2010, 38: 7485-7499
CrossRef Google scholar
[73]
UshikiN, FujitaniH, AoiY, TsunedaS. Isolation of Nitrospira belonging to sublineage II from a wastewater treatment plant. Microbes Environ, 2013, 28: 346-353
CrossRef Google scholar
[74]
WangQ, GarrityGM, TiedjeJM, ColeJR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol, 2007, 73: 5261-5267
CrossRef Google scholar
[75]
WillettesHJ. The survival of fungal sclerotia under adverse environmental conditions. Biol Rev, 1971, 46: 387-407
CrossRef Google scholar
[76]
WillettsHJ, BullockS. Developmental biology of sclerotia. Mycol Res, 1992, 96: 801-816
CrossRef Google scholar
[77]
XiaoX, FanM, WangE, ChenW, WeiG. Interactions of plant growth-promoting rhizobacteria and soil factors in two leguminous plants. Appl Microbiol Biotechnol, 2017, 101: 8485-8497
CrossRef Google scholar
[78]
YangB, WangY, QianP-Y. Sensitivity and correlation of hypervariable regions in 16S rRNA genes in phylogenetic analysis. BMC Bioinformatics, 2016, 17: 135-142
CrossRef Google scholar
[79]
Yang Y, Wang N, Guo X, Zhang Y, Ye B (2017) Comparative analysis of bacterial community structure in the rhizosphere of maize by high-throughput pyrosequencing. PLoS ONE 12:e0178425. https://doi.org/10.1371/journal.pone.0178425
[80]
YapYH, TanN, FungS, AzizAA, TanC, NgS. Nutrient composition, antioxidant properties, and anti-proliferative activity of Lignosus rhinocerus Cooke sclerotium. J Sci Food Agric, 2013, 93: 2945-2952
CrossRef Google scholar
[81]
Yellareddygari S, Reddy M, Kloepper J, Lawrence K, Fadamiro H (2014) Rice sheath blight: A review of disease and pathogen management approaches. J Plant Pathol Microbiol 05:04. https://doi.org/10.4172/2157-7471.1000241
[82]
YinC, HulbertSH, SchroederKL, MavrodiO, MavrodiD, DhingraA, SchillingerWF, PaulitzTC. Role of bacterial communities in the natural suppression of Rhizoctonia solani bare patch disease of wheat (Triticum aestivum L.). Appl Environ Microbiol, 2013, 79: 7428-7438
CrossRef Google scholar
[83]
YuY, SunH, XiaZ. Progress on biological control of rice sheath blight. Mol Plant Breed, 2019, 17: 600-605
[84]
ZhangS, YangY, LiK. Occurrence and control against rice sheath blight. Biol Dis Sci, 2019, 42: 87-91
[85]
ZhaoY, GaoZ, TianB, BiK, ChenT, LiuH, XieJ, ChengJ, FuY, JiangD. Endosphere microbiome comparison between symptomatic and asymptomatic roots of Brassica napus infected with Plasmodiophora brassicae. PLoS ONE, 2017, 12: 1-19
CrossRef Google scholar
[86]
ZhouE, YangM, LiL, ZengW. The effects of media on the mycelial growth and sclerotial formation of Rhizoctonia solani AG-1-IA. J South China Agric Univ, 2002, 23: 33-35
[87]
ZhuG, LiangE, LanX, LiQ, QianJJ, TaoHX, ZhangMJ, XiaoN, ZuoSM, ChenJM, GaoY. ZmPGIP3 gene encodes a polygalacturonase-inhibiting protein that enhances resistance to sheath blight in rice. Phytopathology, 2019, 109: 1732-1740
CrossRef Google scholar
Funding
China Agriculture Research System of MOF and MARA(-)

Accesses

Citations

Detail

Sections
Recommended

/