Abstract
This study aimed to evaluate the resilience of phytophysiognomies under influence of iron mining by assessing the occurrence, diversity, and symbiotic efficiency of native communities of nitrogen-fixing bacteria that nodulate leguminous plants (rhizobia) in soils of an area revegetated with grass after iron mining activities and in the phytophysiognomies in adjacent areas (Canga, Atlantic Forest, Cerrado, and Eucalyptus-planted forest). Experiments for capturing rhizobia through two species of promiscuous plants, siratro (Macroptilium atropurpureum) and cowpea (Vigna unguiculata), were conducted in a greenhouse. The rhizobial strains isolated were characterized phenotypically, genetically (16S rRNA sequencing and BOX-PCR fingerprinting), and regard symbiotic efficiency of biological nitrogen fixation (BNF) compared to mineral nitrogen and reference strains. Cowpea captured a higher density of rhizobia than siratro did. However, most of the strains captured by siratro had greater symbiotic efficiency. The revegetated area proved to be the community most efficient in N2 fixation and was also the most diverse, whereas Canga was the least diverse. For the two trap species, the predominant genus captured in the revegetated area and in the phytophysiognomies was Bradyrhizobium. The greater symbiotic efficiency and the high genetic diversity of the rhizobial community in the revegetated area indicate the effectiveness of the soil rehabilitation process. The revegetated area and the phytophysiognomies proved to harbor strains with high biotechnological potential. Results indicate that the high functional redundancy of this group of bacteria contributes to the resilience of these phytophysiognomies and the revegetated area.
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References
Skirycz A, Castilho A, Chaparro C, Carvalho N, Tzotzos G, Siqueira JO (2014) Canga biodiversity, a matter of mining. Front Plant Sci 5:1–9. https://doi.org/10.3389/fpls.2014.00653
Teixeira AFS, Silva SHG, Carvalho TS, Silva AO, Guimarães AA, Moreira FMS (2021) Soil physicochemical properties and terrain information predict soil enzymes activity in phytophysiognomies of the Quadrilátero Ferrífero region in Brazil. CATENA 199:105083. https://doi.org/10.1016/j.catena.2020.105083
Trindade FC, Ramos SJ, Gastauer M, Saraiva AMM, Caldeira CF, Oliveira G, Valadares RBS (2020) Metaproteomes reveal increased capacity for stress tolerance of soil microbes in ferruginous tropical rocky outcrops. Pedobiologia 81–82:150664. https://doi.org/10.1016/j.pedobi.2020.150664
Farrell M, Griffith GW, Hobbs PJ, Perkins WT, Jones DL (2010) Microbial diversity and activity are increased by compost amendment of metal-contaminated soil. FEMS Microbiol Ecol 71:94–105. https://doi.org/10.1111/j.1574-6941.2009.00793.x
Couto FR, Ferreira AM, Pontes PP, Marques AR (2021) Physical, chemical, and microbiological characterization of the soils contaminated by iron ore tailing mud after Fundão Dam disaster in Brazil. Appl Soil Ecol 158:103811. https://doi.org/10.1016/j.apsoil.2020.103811
Gastauer M, Caldeira CF, Ramos SJ, Trevelin LC, Jaffé R, Oliveira G, Vera MPO, Pires E, Santiago FLA, Carneiro MAC, Coelho FTA, Silva R, Souza-Filho PWM, Siqueira JO (2020) Integrating environmental variables by multivariate ordination enables the reliable estimation of mineland rehabilitation status. J Environ Manag 256:109894. https://doi.org/10.1016/j.jenvman.2019.109894
Szwedzicki T (2001) Program for mine closure. Miner Res Eng 10:347–364. https://doi.org/10.1142/S0950609801000701
Silva AO, Guimarães AA, Costa AM, Rodrigues TL, Carvalho TS, Sales FR, Moreira FMS (2020) Plant growth-promoting rhizobacterial communities from an area under the influence of iron mining and from the adjacent phytophysiognomies have high genetic diversity. Land Degrad Dev 31:2237–2254. https://doi.org/10.1002/ldr.3593
Moreira FMS (2006) Nitrogen-fixing Leguminosae-nodulating bacteria. In: Moreira FMS, Siqueira JO, Brussaard L (eds) Soil biodiversity in Amazonian and other Brazilian ecosystems. CAB International, Wallingford, pp 237–270
Costa EM, Ribeiro PRA, Carvalho TS, Vicentin RP, Balsanelli E, Souza EM, Lebbe L, Willems A, Moreira FMS (2020) Efficient nitrogen-fixing bacteria isolated from soybean nodules in the semi-arid region of Northeast Brazil are classified as Bradyrhizobium brasilense (Symbiovar Sojae). Curr Microbiol 77:1746–1755. https://doi.org/10.1007/s00284-020-01993-6
Rangel WM, Oliveira-Longatti SM, Ferreira PAA, Bonaldi DS, Guimarães AA, Thijs S, Weyens N, Vangronsveld J, Moreira FMS (2017) Leguminosae native nodulating bacteria from a gold mine As-contaminated soil: multi-resistance to trace elements, and possible role in plant growth and mineral nutrition. Int J Phytoremediat 19:925–936. https://doi.org/10.1080/15226514.2017.1303812
Teixeira AFS, Kemmelmeier K, Marascalchi MN, Stürmer SL, Carneiro MAC, Moreira FMS (2017) Arbuscular mycorrhizal fungal communities in an iron mining area and its surroundings: inoculum potential, density, and diversity of spores related to soil properties. Ciênc Agrotec 41:511–525. https://doi.org/10.1590/1413-70542017415014617
Castro JL, Souza MG, Rufini M, Guimarães AA, Rodrigues TL, Moreira FMS (2017) Diversity and efficiency of rhizobia communities from iron mining areas using cowpea as a trap plant. Rev Bras Ciênc Solo. https://doi.org/10.1590/18069657rbcs20160525
Odori C, Ngaira J, Kinyua J, Nyaboga EN (2020) Morphological, genetic diversity and symbiotic functioning of rhizobia isolates nodulating cowpea (Vigna unguiculata L. Walp) in soils of Western Kenya and their tolerance to abiotic stress. Cogent Food Agric. https://doi.org/10.1080/23311932.2020.1853009
Rocha SMB, Mendes LW, Oliveira LMS, Melo VMM, Antunes JEL, Araujo FF, Hungria M, Araujo ASF (2020) Nodule microbiome from cowpea and lima bean grown in composted tannery sludge-treated soil. Appl Soil Ecol 151:103542. https://doi.org/10.1016/j.apsoil.2020.103542
Zilli JE, Valisheski RR, Freire Filho FR, Neves MCP, Rumjanek NG (2004) Assessment of cowpea rhizobium diversity in Cerrado areas of northeastern Brazil. Braz J Microbiol 35:281–287. https://doi.org/10.1590/S1517-83822004000300002
Borges WL, Prin Y, Ducousso M, Le Roux C, Faria SM (2016) Rhizobial characterization in revegetated areas after bauxite mining. Braz J Microbiol 47:314–321. https://doi.org/10.1016/j.bjm.2016.01.009
Lima AS, Nóbrega RSA, Barberi A, Silva K, Ferreira DF, Moreira FMS (2009) Nitrogen-fixing bacteria communities occurring in soils under different uses in the Western Amazon Region as indicated by nodulation of siratro (Macroptilium atropurpureum). Plant Soil 319:127–145. https://doi.org/10.1007/s11104-008-9855-2
Felestrino EB, Vieira IT, Caneschi WL, Cordeiro IF, Assis RAB, Lemes CGC, Fonseca NP, Sanchez AB, Cepeda JCC, Ferro JA, Garcia CCM, Carmo FF, Kamino LHY, Moreira LM (2018) Biotechnological potential of plant growth-promoting bactéria from the roots and rhizospheres of endemic plants in ironstone vegetation in southeastern Brazil. World J Microbiol Biotechnol 34:1–14. https://doi.org/10.1007/s11274-018-2538-0
Guimarães AA, Jaramillo PMD, Nóbrega RSA, Florentino LA, Silva KB, Moreira FMS (2012) Genetic and symbiotic diversity of nitrogen-fixing bacteria isolated from agricultural soils in the western Amazon by using cowpea as the trap plant. J Appl Environ Microbiol 78:6726–6733. https://doi.org/10.1128/AEM.01303-12
Jaramillo PMD, Guimarães AA, Florentino LA, Silva KB, Nóbrega RSA, Moreira FMS (2013) Symbiotic nitrogen-fixing bacterial populations trapped from soils under agroforestry systems in the Western Amazon. Sci Agric 70:397–404. https://doi.org/10.1590/S0103-90162013000600004
Oliveira DP, Soares BL, Ferreira PAA, Passos TR, Silva JS, Ferreira DF, Andrade MJB, Moreira FMS (2020) Selection of elite Bradyrhizobium strains by biometric techniques for inoculation in cowpea. Soil Sci Soc Am J 84:1125–1138. https://doi.org/10.1002/saj2.20084
Ormeño-Orrillo E, Rogel-Hernández MA, Lloret L, López-López A, Martínez J, Barois I, Martínez-Romero E (2012) Change in land use alters the diversity and composition of Bradyrhizobium communities and led to the introduction of Rhizobium etli into the tropical rain forest of Los Tuxtlas (Mexico). Microb Ecol 63:822–834. https://doi.org/10.1007/s00248-011-9974-9
Soares ALL, Pereira JPAR, Ferreira PAA, Vale HMM, Lima AS, Andrade MJB, Moreira FMS (2006) Eficiência agronômica de rizóbios selecionados e diversidade de populações nativas nodulíferas em perdões (MG). I – caupi. Rev Bras Ciênc Solo 30:795–802. https://doi.org/10.1590/S0100-06832006000500005
Ndungu SM, Messmer MM, Ziegler D, Gamper HA, Mészáros E, Thuita M, Vanlauwe B, Frossard E, Thonar C (2018) Cowpea (Vigna unguiculata L. Walp) hosts several widespread bradyrhizobial root nodule symbionts across contrasting agro-ecological production areas in Kenya. Agric Ecosyst Environ 261:161–171. https://doi.org/10.1016/j.agee.2017.12.014
Ribeiro PRA, Santos JV, Costa EM, Lebbe L, Assis ES, Louzada MO, Guimarães AA, Willems A, Moreira FMS (2015) Symbiotic efficiency and genetic diversity of soybean bradyrhizobia in Brazilian soils. Agric Ecosyst Environ 212:85–93. https://doi.org/10.1016/j.agee.2015.06.017
Matias SR, Pagano MC, Muzzi FC, Oliveira CA, Carneiro AA, Horta SN, Scotti MR (2009) Effect of rhizobia, mycorrhizal fungi and phosphate-solubilizing microorganisms in the rhizosphere of native plants used to recover an iron ore area in Brazil. Eur J Soil Biol 45:259–266. https://doi.org/10.1016/j.ejsobi.2009.02.003
Hoagland D, Arnon DI (1950) The water culture method for growing plants without soil. California Agricultural Experiment Station, Circular No 347. University of California, Berkeley
Costa EM, Guimarães AA, Vicentin RP, Ribeiro PRA, Leão ACR, Balsanelli E, Lebbe L, Aerts M, Willems A, Moreira FMS (2017) Bradyrhizobium brasilense sp. nov., a symbiotic nitrogen-fixing bacterium isolated from Brazilian tropical soils. Arch Microbiol 199:1211–1221. https://doi.org/10.1007/s00203-017-1390-1
Costa EM, Carvalho TS, Guimarães AA, Leão ACR, Cruz LM, Baura VA, Lebbe L, Willems A, Moreira FMS (2019) Classification of the inoculant strain of cowpea UFLA03-84 and of other strains from soils of the Amazon region as Bradyrhizobium viridifuturi (symbiovar tropici). Braz J Microbiol 50:1–12. https://doi.org/10.1007/s42770-019-00045-x
Fred EB, Waksman SA (1928) Laboratory manual of general microbiology. McGraw-Hill, New York
Niemann S, Puehler A, Tichy HV, Simon R, Selbitshka W (1997) Evaluation of the resolving power of three different DNA fingerprinting methods to discriminate among isolates of a natural Rhizobium meliloti population. J Appl Microbiol 82:477–484. https://doi.org/10.1046/j.1365-2672.1997.00141.x
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–148
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687. https://doi.org/10.1093/oxfordjournals.molbev.a040752
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Versalovic J, Schneider GM, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence based polymerase chain reaction. Methods Mol Cell Biol 5:25–40
R Development Core Team (2020) R: a language and environment for statistical computing. R foundation for statistical computing. https://www.R-project.org/
Moreira FM, Silva MF, Faria SM (1992) Occurrence of nodulation in legume species in the Amazon region of Brazil. New Phytol 121:563–570. https://doi.org/10.1111/j.1469-8137.1992.tb01126.x
Melloni R, Moreira FMS, Nóbrega RSA, Siqueira JO (2006) Eficiência e diversidade fenotípica de bactérias diazotróficas que nodulam caupi [Vigna unguiculata (L.) WALP] e feijoeiro (Phaseolus vulgaris L.) em solos de mineração de bauxita em reabilitação. Rev Bras Ciênc Solo 30:235–246. https://doi.org/10.1590/S0100-06832006000200005
Moreira FMS, Gillis M, Pot B, Kersters K, Franco AA (1993) Characterization of rhizobia isolated from different divergence groups of tropical leguminosae by comparative polyacrylamide gel electrophoresis of their total proteins. Syst Appl Microbiol 16:135–146. https://doi.org/10.1016/S0723-2020(11)80258-4
Santos JMF, Alves PAC, Silva VC, Ferreira M, Rhem K, James EK, Gross E (2017) Diverse genotypes of Bradyrhizobium nodulate herbaceous Chamaecrista (Moench) (Fabaceae, Caesalpinioideae) species in Brazil. Syst Appl Microbiol 40:69–79. https://doi.org/10.1016/j.syapm.2016.12.004
Carvalho Filho A, Inda AV, Fink JR, Curi N (2015) Iron oxides in soils of different lithological origins in Ferriferous Quadrilateral (Minas Gerais, Brazil). Appl Clay Sci 118:1–7. https://doi.org/10.1016/j.clay.2015.08.037
Silva AO, Costa AM, Teixeira AFS, Guimarães AA, Santos JV, Moreira FMS (2018) Soil microbiological attributes indicate recovery of an iron mining area and of the biological quality of adjacent phytophysiognomies. Ecol Indic 93:142–151. https://doi.org/10.1016/j.ecolind.2018.04.073
Avontuur JR, Palmer M, Beukes CW, Chan WY, Coetzee MPA, Blom J, Stępkowski T, Kyrpides NC, Woyke T, Shapiro N, Whitman WB, Venter SN, Steenkamp ET (2019) Genome-informed Bradyrhizobium taxonomy: where to from here? Syst Appl Microbiol 42:427–439. https://doi.org/10.1016/j.syapm.2019.03.006
Sy A, Giraud E, Jourand P, Garcia N, Willems A, Lajudiel P, Prin Y, Neyral M, Gillis M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220. https://doi.org/10.1128/JB.183.1.214-220.2001
Kwak Y, Shin JH (2015) Complete genome sequence of Paenibacillus beijingensis 7188(T) (=DSM 24997(T)), a novel rhizobacterium from jujube garden soil. J Biotechnol 206:75–76. https://doi.org/10.1016/j.jbiotec.2015.04.015
Andam CP, Parker MA (2007) Novel alphaproteobacterial root nodule symbiont associated with Lupinus texensis. Appl Environ Microbiol 73:5687–5691. https://doi.org/10.1128/AEM.01413-07
Zhang WT, Yang JK, Yuan TY, Zhou JC (2007) Genetic diversity and phylogeny of indigenous rhizobia from cowpea [Vigna unguiculata (L.) Walp.]. Biol Fertil Soils 44:201–210. https://doi.org/10.1007/s00374-007-0196-8
Han S, Delgado-Baquerizo M, Luo X, Liu Y, Van Nostrand JD, Chen W, Zhou J, Huang Q (2021) Soil aggregate size-dependent relationships between microbial functional diversity and multifunctionality. Soil Biol Biochem 154:108143. https://doi.org/10.1016/j.soilbio.2021.108143
Manual de análises químicas de solos, plantas e fertilizantes/editor técnico (2009) Fábio Cesar da Silva. – 2. ed. rev. ampl. - Brasília, DF: Embrapa Informação Tecnológica, p 627
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We are grateful for the financial support provided for the project CRA-RDP-00136–10 (FAPEMIG/FAPESP/FAPESPA/Vale S.A) and express our thanks to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes/PROEX AUXPE 593–2018), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and the Fundação de Amparo à Pesquisa de Minas Gerais (Fapemig) for the financial support and scholarships granted to the authors.
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All authors PFC, AOS, AAG, LLRdA, MR, LdPB, TSdC, and FMdSM have contributed for Conceptualization, Data acquisition, Data analysis, and Writing and editing of the manuscript.
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Supplementary file1 (PDF 269 kb). Fig. S1 Maximum likelihood phylogenetic tree based on the 16S rRNA gene sequences (1010 bp) of rhizobia species type strains and strains isolated from nodules of siratro (Macroptilium atropurpureum) and cowpea (Vigna unguiculata) plants that were inoculated with soil samples collected from Atlantic Forest, Canga (Ironstone Outcrops), Cerrado, Eucalyptus, and a Revegetated Area revegetated with grass in the Quadrilátero Ferrífero, MG, Brazil. Bootstrap values were based on 1000 trials. All positions containing gaps and missing data were eliminated from the dataset. Bootstrap values >70% are indicated at the nodes. Phylogenetic analyses were conducted in Mega5. Strains that showed high efficiency in nitrogen fixation are highlighted in bold
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Freitas Costa, P., Oliveira Silva, A., Azarias Guimarães, A. et al. Diversity and Efficiency of Rhizobia from a Revegetated Area and Hotspot-Phytophysiognomies Affected by Iron Mining as Indicators of Rehabilitation and Biotechnological Potential. Curr Microbiol 80, 40 (2023). https://doi.org/10.1007/s00284-022-03104-z
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DOI: https://doi.org/10.1007/s00284-022-03104-z