Abstract
The potential nitrogen-fixing bacterial diversity in the rhizospheric soil of the native switchgrass (Panicum virgatum L.) from Tall Grass Prairies of Northern Oklahoma was studied using a partial region of nitrogenase structural gene—nifH. Eleven clone libraries constructed from nifH amplicons gave 407 good-quality sequences. More than 70% of sequences showed similarity of nifH with uncultured bacteria (< 98%). The dominance of sequences affiliated with Deltaproteobacterial nifH was observed, followed by Betaproteobacterial nifH sequences. The nifH gene library was dominated by the genera Geobacter, Rhizobacter, Paenibacillus, and Azoarcus. Sequences affiliated with rhizobia, such as Bradyrhizobium, Methylocystis, Ensifer, etc., were also in the rhizosphere in small numbers. From Deltaproteobacteria, five genera, namely Geobacter, Pelobacter, Geomonas, Desulfovibrio, and Anaeromyxobacter, contributed to 48% of the total sequences suggesting the dominance of group Deltaproteobacteria in the rhizosphere of native switchgrass. Considering the percent similarity of the nifH sequences with cultivated bacteria, this study demonstrated the presence of novel bacterial species in switchgrass rhizospheric soil from Tall Grass Prairie.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410
Amann RI, Ludwig W, Schleifer K (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
Bahulikar RA, Torres-Jerez I, Worley E, Craven K, Udvardi MK (2014) Diversity of nitrogen-fixing bacteria associated with switchgrass in the native tall-grass prairie of Northern Oklahoma. Appl Environ Microbiol 80(18):5636–5643
Bahulikar RA, Chaluvadi SR, Torres-Jerez I, Mosali J, Bennetzen JL, Udvardi M (2021) Nitrogen fertilization reduces nitrogen fixation activity of diverse diazotrophs in switchgrass roots. Phytobiomes J 5(1):80–87
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486
Bernabeu PR, Garcia SS, Lopez AC, Vio SA, Carrasco N, Boiardi JL, Luna MF (2018) Assessment of bacterial inoculant formulated with Paraburkholderia tropica to enhance wheat productivity. World J Microbiol Biotechnol 34(6):81. https://doi.org/10.1007/s11274-018-2461-4
Bouton J (2008) Improvement of switchgrass as a bioenergy crop. In: Vermerris W (ed) Genetic improvement of bioenergy crops. Spinger Science and Business Media, pp 295–308
Casler MD, Vogel KP, Taliaferro CM, Ehlke NJ, Berdahl JD, Brummer EC, Kallenbach RL, West CP, Mitchell RB (2007) Latitudinal and longitudinal adaptation of switchgrass populations. Crop Sci 47(6):2249–2260. https://doi.org/10.2135/cropsci2006.12.0780
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209(2):798–811. https://doi.org/10.1111/nph.13697
Gaby JC, Buckley DH (2011) A global census of nitrogenase diversity. Environ Microbiol 13(7):1790–1799. https://doi.org/10.1111/j.1462-2920.2011.02488.x
Ghimire SR, Charlton ND, Bell JD, Krishnamurthy YL, Craven KD (2011) Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L.) growing in the native tallgrass prairie of northern Oklahoma. Fungal Divers 47(1):19–27. https://doi.org/10.1007/s13225-010-0085-6
Guretzky JA, Biermacher JT, Cook BJ, Kering MK, Mosali J (2010) Switchgrass for forage and bioenergy: harvest and nitrogen rate effects on biomass yields and nutrient composition. Plant Soil 339(1–2):69–81
Hammer Ø, Harper DAT, Ryan PD (2001) Past: Paleontological statistics software package for education and data analysis. Palaeontol Electron. 4(1):4–9
Hestrin R, Lee MR, Whitaker BK, Pett-Ridge J (2021) The switchgrass microbiome: a review of structure, function, and taxonomic distribution. Phytobiomes J. https://doi.org/10.1094/pbiomes-04-20-0029-fi
Jefferson PG, McCaughey WP (2012) Switchgrass (Panicum virgatum L.) cultivar adaptation, biomass production, and cellulose concentration as affected by latitude of origin. ISRN Agronomy 2012:1–9. https://doi.org/10.5402/2012/763046
Katoh K, Toh H (2010) Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26(15):1899–1900. https://doi.org/10.1093/bioinformatics/btq224
Kaur C, Selvakumar G, Ganeshamurthy AN (2016) Draft genome sequence of phosphate-solubilizing bacterium Paraburkholderia tropica strain P-31 isolated from pomegranate (Punica granatum) rhizosphere. Genome Announc. https://doi.org/10.1128/genomeA.00844-16
Ker K, Seguin P, Driscoll BT, Fyles JW, Smith DL (2012) Switchgrass establishment and seeding year production can be improved by inoculation with rhizosphere endophytes. Biomass Bioenerg 47:295–301. https://doi.org/10.1016/j.biombioe.2012.09.031
Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, von Mering C, Vorholt JA (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6(7):1378–1390. https://doi.org/10.1038/ismej.2011.192
Lemus R, Parrish DJ, Abaye O (2008) Nitrogen-use dynamics in switchgrass grown for biomass. BioEnergy Res 1(2):153–162. https://doi.org/10.1007/s12155-008-9014-x
Lemus R, Parrish DJ, Wolf DD (2009) Nutrient uptake by “Alamo” switchgrass used as an energy crop. BioEnergy Res 2(1–2):37–50. https://doi.org/10.1007/s12155-009-9032-3
Li T, Zhou Q (2020) The key role of Geobacter in regulating emissions and biogeochemical cycling of soil-derived greenhouse gases. Environ Pollut Control 266:115135
Liang C, Jesus EdC, Duncan DS, Quensen JF, Jackson RD, Balser TC, Tiedje JM (2016) Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA. Soil Biol Biochem 94:173–180. https://doi.org/10.1016/j.soilbio.2015.11.020
Martensson L, Diez B, Wartiainen I, Zheng W, El-Shehawy R, Rasmussen U (2009) Diazotrophic diversity, nifH gene expression and nitrogenase activity in a rice paddy field in Fujian. China Plant Soil 325(1–2):207–218. https://doi.org/10.1007/s11104-009-9970-8
Masuda Y, Itoh H, Shiratori Y, Isobe K, Otsuka S, Senoo K (2017) Predominant but previously-overlooked prokaryotic drivers of reductive nitrogen transformation in paddy soils, revealed by metatranscriptomics. Microbes and Environ 32(2):180–183
Nicholas KB Jr, Nicholas HB, Deerfield DWI (1997) GeneDoc: Analysis and visualization of genetic variation. EMBNEWNEWS 4:14
Parrish DJ, Fike JH (2005) The biology and agronomy of switchgrass for biofuels. Crit Rev Plant Sci 24(5–6):423–459. https://doi.org/10.1080/07352680500316433
Parrish DJ, Fike JH (2009) Selecting, establishing, and managing switchgrass (Panicum virgatum) for biofuels. Biofuels Methods Protoc. https://doi.org/10.1007/978-1-60761-214-8_2
Revillini D, Wilson GWT, Miller RM, Lancione R, Johnson NC (2019) Plant diversity and fertilizer management shape the belowground microbiome of native grass bioenergy feedstocks. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01018
Rodrigues Coelho MR, De Vos M, Carneiro NP, Marriel IE, Paiva E, Seldin L (2008) Diversity of nifH gene pools in the rhizosphere of two cultivars of sorghum (Sorghum bicolor) treated with contrasting levels of nitrogen fertilizer. FEMS Microbiol Lett 279(1):15–22
Roesch LFW, Camargo FAO, Bento FM, Triplett EW (2008) Biodiversity of diazotrophic bacteria within the soil, root and stem of field-grown maize. Plant Soil 302(1–2):91–104
Roley SS, Duncan DS, Liang D, Garoutte A, Randall Jackson D, Tiedje JM, Robertson GP (2018) Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient. PLoS One 13:e0197320. https://doi.org/10.1371/journal.pone.0197320
Roley SS, Xue C, Hamilton SK, Tiedje JM, Robertson GP (2019) Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.). Soil Biol Biochem 129:90–98. https://doi.org/10.1016/j.soilbio.2018.11.006
Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 5:429. https://doi.org/10.3389/fgene.2014.00429
Sessitsch A, Hardoim P, Doering J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25(1):28–36. https://doi.org/10.1094/mpmi-08-11-0204
Shanta N, Schwinghamer T, Backer R, Allaire SE, Teshler I, Vanasse A, Whalen J, Baril B, Lange S, MacKay J, Zhou X, Smith DL (2016) Biochar and plant growth promoting rhizobacteria effects on switchgrass (Panicum virgatum cv. cave-in-rock) for biomass production in southern Québec depend on soil type and location. Biomass Bioenerg 95:167–173. https://doi.org/10.1016/j.biombioe.2016.10.005
Shu W, Pablo GP, Jun Y, Danfeng H (2012) Abundance and diversity of nitrogen-fixing bacteria in rhizosphere and bulk paddy soil under different duration of organic management. World J Microbiol Biotechnol 28(2):493–503
Silva P, Simoes-Araujo JL, Vidal MS, Cruz LM, Souza EM, Baldani JI (2018) Draft genome sequence of Paraburkholderia tropica Ppe8 strain, a sugarcane endophytic diazotrophic bacterium. Braz J Microbiol 49(2):210–211. https://doi.org/10.1016/j.bjm.2017.07.005
Smercina DN, Evans SE, Friesen ML, Tiemann LK (2021) Temporal dynamics of free-living nitrogen fixation in the switchgrass rhizosphere. GCB Bioenergy 13(11):1814–1830. https://doi.org/10.1111/gcbb.12893
Spiertz JHJ (2010) Nitrogen, sustainable agriculture and food security. A review. Agron Sustain Dev (EDP Sciences) 30(1):43–55. https://doi.org/10.1051/agro:2008064
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. https://doi.org/10.1093/molbev/msr121
Tjepkema JD, Burris RH (1976) Nitrogenase activity associated with some Wisconsin prairie grasses. Plant Soil 45(1):81–94. https://doi.org/10.1007/bf00011131
Watve M, Shejval V, Sonawane C, Rahalkar M, Matapurkar A, Shouche Y, Patole M, Phadnis N, Champhenkar A, Damle K, Karandikar S, Kshirsagar V, Jog M (2000) The “K” selected oligophilic bacteria: a key to uncultured diversity? Curr Sci 78(12):1535–1542
Weese DJ, Heath KD, Dentinger BT, Lau JA (2015) Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution 69(3):631–642
Xu Z, Masuda Y, Itoh H, Ushijima N, Shiratori Y, Senoo K (2019) Geomonas oryzae gen. nov., sp. nov., Geomonas edaphica sp. nov., Geomonas ferrireducens sp. nov., Geomonas terrae sp. nov., four ferric-reducing bacteria isolated from paddy soil, and reclassification of three species of the genus Geobacter as members of the genus Geomonas gen. nov. Front Microbiol 10:2201. https://doi.org/10.3389/fmicb.2019.02201
Yang JD, Worley E, Wang MY, Lahner B, Salt DE, Saha M, Udvardi M (2009) Natural variation for nutrient use and remobilization efficiencies in switchgrass. BioEnergy Res 2(4):257–266. https://doi.org/10.1007/s12155-009-9055-9
Yu Y, Breitbart M, McNairnie P, Rohwer F (2006) FastGroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinform 7:57
Zani S, Mellon MT, Collier JL, Zehr JP (2000) Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR. Appl Environ Microbiol 66(7):3119–3124
Acknowledgements
I thank the Genomics/Microarray Facility at The Noble Research Institute for sequencing nifH. I also thank Michel Udvardi for allowing me to work on this aspect.
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The Noble Research Institute, OK, USA financially supported this work.
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Bahulikar, R.A. Prevalence of Deltaproteobacterial sequences in nifH gene pools associated with the rhizosphere of native switchgrass from Tall Grass Prairie (Oklahoma, USA). 3 Biotech 13, 210 (2023). https://doi.org/10.1007/s13205-023-03640-w
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DOI: https://doi.org/10.1007/s13205-023-03640-w