Skip to main content
Log in

Soil characteristics determine the rhizobia in association with different species of Mimosa in central Brazil

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

To evaluate the influence of soil type on the symbiosis between Mimosa spp. and rhizobia.

Methods

A greenhouse experiment was carried out with trap plants using seeds of six species of Mimosa and soils from three different locations in central Brazil: Posse, Brasília and Cavalcante. Plant dry biomass and number of nodules were measured after four months. Symbiotic bacteria were isolated from nodules and their molecular identification was performed. Three housekeeping genes (16S rRNA, recA and gyrB) plus the nodC and nifH symbiotic genes were used to determine the identity of the symbionts and to reconstruct the phylogenetic relationships among the isolated nitrogen-fixing bacteria.

Results

Rhizobia from the Betaproteobacterial genus Paraburkholderia (former Burkholderia) and the Alphaproteobacterial genus Rhizobium were isolated from different species of Mimosa. As in previous studies, the phylogenies of their symbiosis-essential genes, nodC and nifH, were broadly congruent with their core housekeeping genes (16S rRNA, recA and gyrB), which suggests limited or no horizontal gene transfer. Edaphic factors such as pH and fertility influenced the occurrence of these unrelated rhizobial types in the nodules on these Mimosa spp.

Conclusions

Mimosa species have the ability to associate with different types of rhizobia (α- and β-proteobacteria), suggesting low specificity between host and bacterium in experimental conditions. Soil factors such as pH, nitrogen and fertility seem to favour the predominance of certain types of rhizobia, thus influencing the establishment of symbiotic relationships.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Araújo JF, de Castro AP, Costa MM, Togawa RC, Junior GJ, Quirino BF, Bustamante MMC, Williamson L, Handelsman J, Krüger RH (2012) Characterization of soil bacterial assemblies in Brazilian savanna-like vegetation reveals acido bacteria dominance. Microb Ecol 64:760–770

    Article  PubMed  Google Scholar 

  • Baraúna AC, Rouws LFM, Simoes-Araujo JL, dos Reis Junior FB, Iannetta PP, Maluk M, Goi SR, Reis VM, James EK, Zilli JE (2016) Rhizobium altiplani sp. nov. isolated from effective nodules on Mimosa pudica growing in untypically alkaline soil in Central Brazil. Int J Syst Evol Microbiol 66:1–7

    Article  Google Scholar 

  • Barneby RC (1991) Sensitivae Censitae: a description of the genus Mimosa Linnaeus (Mimosaceae) in the new world. Mem N Y Bot Gard 65:1–835

    Google Scholar 

  • Barrett CF, Parker MA (2006) Coexistence of Burkholderia, Cupriavidus and Rhizobium sp. nodule bacteria on two Mimosa species in Costa Rica. Appl Environ Microbiol 72:1198–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beukes CW, Venter SN, Law IJ, Phalane FL, Steenkamp ET (2013) South African papilonoid legumes are nodulated by diverse Burkholderia with unique nodulation and nitrogen-fixation loci. PLoS One 8:e68406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beukes C, Palmer M, Manyaka P, Chan WY, Avontuur J, Zyl E, Huntemann M, Clum A, Pillay M, Palaniappan K, Varghese N, Mikhailova N, Stamatis D, Reddy TBK, Daum C, Shapiro N, Markowitz V, Ivanova N, Kyrpides N, Woyke T, Blom J, Whitman WB, Venter SN, Steenkamp ET (2017) Genome data provides high support for generic boundaries in Burkholderia sensu lato. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01154

  • Bontemps C, Elliott GN, Simon MF, dos Reis Junior FB, Gross E, Lawton RC, Neto NE, Loureiro MF, de Faria SM, Sprent JI, James EK, Young JPW (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52

    Article  CAS  PubMed  Google Scholar 

  • Bontemps C, Rogel MA, Wiechmann A, Mussabekova A, Moody S, Simon MF, Moulin L, Elliott GN, Lacercat-Didier L, Da Silva C, Grether R, Camargo-Ricalde SL, Chen W, Sprent JI, Martínez-Romero E, Young JPW, James EK (2016) Endemic Mimosa species from Mexico prefer alphaproteobacterial rhizobial symbionts. New Phytol 209:319–333

    Article  CAS  PubMed  Google Scholar 

  • Bournaud C, de Faria SM, dos Santos JMF, Tisseyre P, Silva M, Chaintreuil C, Gross E, James EK, Prin Y, Moulin L (2013) Burkholderia species are the most common and preferred nodulating symbionts of the Piptadenia group (tribe Mimoseae). PLoS One 8:e63478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro AP, Silva MRSS, Quirino BF, Bustamante MMC, Krüger RH (2016) Microbial diversity in Cerrado biome (Neotropical savanna) soils. PLoS One 11:e0148785

    Article  PubMed  Google Scholar 

  • Chen WM, Laevens S, Lee TM, Coenye T, De Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, James EK, Prescott AR, Kierans M, Sprent JI (2003) Nodulation of Mimosa spp. by the β-proteobacterium Ralstonia taiwanensis. Mol Plant-Microbe Interact 16:1051–1061

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, de Faria SM, Straliotto R, Pitard RM, Simoes-Araujo JL, Chou JH, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young JPW, James EK (2005a) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Appl Environ Microbiol 71:7461–7471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WM, James EU, Chou JH, Sheu SY, Yang SZ, Sprent JI (2005b) β-rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytol 168:661–675

    Article  CAS  PubMed  Google Scholar 

  • Chen W-M, James EK, Coenye T, Chou J-H, Barrios E, de Faria SM, Elliott GN, Sheu S-H, Sprent JI, Vandamme P (2006) Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int J Syst Evol Microbiol 56:1847–1851

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, de Faria SM, James EK, Elliott GN, Lin KY, Chou JH, Sheu SY, Cnockaert M, Sprent JI, Vandamme P (2007) Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int J Syst Evol Microbiol 57:1055–1059

    Article  CAS  PubMed  Google Scholar 

  • Dall'Agnol RF, Plotegher F, Souza RC, Mendes IC, dos Reis Junior FB, Béna G, Moulin L, Hungria M (2016) Paraburkholderia nodosa is the main N2-fixing species trapped by promiscuous common bean (Phaseolus vulgaris L.) in the Brazilian ‘Cerradão’. FEMS Microbiol Ecol 92: fiw108

  • De Meyer SE, Cnockaert M, Ardley JK, Maker G, Yates R, Howieson JG, Vandamme P (2013) Burkholderia sprentiae sp. nov., isolated from Lebeckia ambigua root nodules. Int J Syst Evol Microbiol 6:3950–3957

    Article  Google Scholar 

  • De Meyer SE, Briscoe L, Martínez-Hidalgo P, Agapakis CM, de-los Santos PE, Seshadri R, Reeve W, Weinstock G, O’Hara G, Howieson JG, Hirsch AM (2016) Symbiotic Burkholderia species show diverse arrangements of nif/fix and nod genes and lack typical high-affinity cytochrome cbb3 oxidase genes. Mol Plant-Microbe Interact 29:609–619

    Article  PubMed  Google Scholar 

  • Elliott GN, Chen W-M, Chou J-H, Wang H-C, Sheu S-Y, Perin L, Reis VM, Moulin L, Simon MF, Bontemps C, Sutherland JM, Bessi R, de Faria SM, Trinick MJ, Prescott AR, Sprent JI, James EK (2007a) Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol 173:168–180

    Article  CAS  PubMed  Google Scholar 

  • Elliott GN, Chen WM, Bontemps C, Chou JH, Young JPW, Sprent JI, James EK (2007b) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Ann Bot 100:1403–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elliott GN, Chou J-H, Chen WM, Bloemberg GV, Bontemps C, Martínez-Romero E, Velázquez E, Young JPW, Sprent JI, James EK (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 11:762–778

    Article  PubMed  Google Scholar 

  • Embrapa (1997) Manual de métodos de análise de solo. 2ª ed. Centro Nacional de Pesquisa de Solos, Rio de Janeiro, p 212

  • Estrada-de los Santos P, Rojas-Rojas FU, Tapia-Garcıa EY, Vásquez-Murrieta MS, Hirsch AM (2016) To split or not to split: an opinion on dividing the genus Burkholderia. Ann Microbiol 66:1303–1314

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Fred EB, Waskman SA (1928) Yeast extract-manitol agar. Laboratory manual of general microbiology. McGraw-Hill, New York, p 145

    Google Scholar 

  • Garau G, Yates R, Deiana P, Howieson JG (2009) Novel strains of nodulating Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soil. Soil Biol Biochem 41:125–134

    Article  CAS  Google Scholar 

  • Gehlot HS, Tak N, Kaushik M, Mitra S, Chen WM, Poweleit N, Panwar D, Poonar N, Parihar R, Tak A, Sankhla IU, Ojha A, Rao SR, Simon MF, Reis Junior FB, Perigolo N, Tripathi AK, Sprent JI, Young JPW, James EK, Gyaneshwar P (2013) An invasive Mimosa in India does not adopt the symbionts of its native relatives. An of Bot 112:179–196

    Article  CAS  Google Scholar 

  • Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-de Los Santos P, Gross E, Reis Junior FB, Sprent JI, Young JPW, James EK (2011) Legume-nodulating betaproteobacteria: diversity, host range and future prospects. Mol Plant-Microbe Interact 24:1276–1288

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95 ⁄ 98 ⁄ NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. California agricultural experimental station. Circ. n.347

  • Howieson JG, De Meyer SE, Vivas-Marfisi A, Ratnayake S, Ardley JK, Yates RJ (2013) Novel Burkholderia bacteria isolated from Lebeckia ambigua - a perennial suffrutescent legume of the fynbos. Soil Biol Biochem 60:55–64

    Article  CAS  Google Scholar 

  • Klonowska A, Chaintreuil C, Tisseyre P, Miché L, Melkonian R, Ducousso M, Laguerre G, Brunel B, Moulin L (2012) Biodiversity of Mimosa pudica rhizobial symbionts (Cupriavidus taiwanensis, Rhizobium mesoamericanum) in New Caledonia and their adaptation to heavy metal-rich soils. FEMS Microbiol Ecol 81:618–635

    Article  CAS  PubMed  Google Scholar 

  • Lammel DR, Cruz LM, Carrer H, Cardoso EJBN (2013) Diversity and symbiotic effectiveness of beta-rhizobia isolated from sub-tropical legumes of a Brazilian Araucaria Forest. World J Microbiol Biotechnol 29:2335–2342

    Article  CAS  PubMed  Google Scholar 

  • Lammel DR, Cruz LM, Mescolotti D, Stürmer SL, Cardoso EJBN (2015) Woody Mimosa species are nodulated by Burkholderia in ombrophylous forest soils and their symbioses are enhanced by arbuscular mycorrhizal fungi (AMF). Plant Soil 393:123–135

  • Lemaire B, Dlodlo O, Chimphango S, Stirton C, Schrire B, Boatwright JS, Honnay O, Smets E, Sprent J, James EK, Muasya AM (2015) Symbiotic diversity, specificity, and distribution of rhizobia in native legumes of the Core cape subregion (South Africa). FEMS Microbiol Ecol 91:1–17

    Article  PubMed  Google Scholar 

  • Lemaire B, Chimphango S, Stirton C, Rafudeen S, Honnay O, Smets E, Chen W-M, Sprent J, James EK, Muasya AM (2016) Biogeographical patterns of legume-nodulating Paraburkholderia: from African Fynbos to continental scales. Appl Environ Microbiol 82:5099–5115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XY, Wei S, Wang F, James EK, Guo XY, Zagar C, Xia LG, Dong X, Wang YP (2012) Burkholderia and Cupriavidus spp. are the preferred symbionts of Mimosa spp. in Southern China. FEMS Microbiol Ecol 80:417–426

    Article  CAS  PubMed  Google Scholar 

  • Liu WYY, Ridgway HJ, James TK, James EK, Chen WM, Sprent JI, Young JPW, Andrews M (2014) Burkholderia sp. induces functional nodules on the South African invasive legume Dipogon lignosus (Phaseoleae) in New Zealand soils. Microb Ecol 68:542–555

    Article  CAS  PubMed  Google Scholar 

  • Melkonian R, Moulin L, Béna G, Tisseyre P, Chaintreuil C, Heulin K, Rezkallah N, Klonowska A, Gonzalez S, Simon M, Chen W-M, James EK, Laguerre G (2014) The geographical patterns of symbiont diversity in the invasive legume Mimosa pudica can be explained by the competitiveness of its symbionts and by the host genotype. Environ Microbiol 16:2099–2111

    Article  PubMed  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA pp 1–8.

  • Mishra RP, Tisseyre P, Melkonian R, Chaintreuil C, Miche L, Klonowska A, Gonzalez S, Bena G, Laguerre G, Moulin L (2012) Genetic diversity of Mimosa pudica rhizobial symbionts in soils of French Guiana: investigating the origin and diversity of Burkholderia phymatum and other beta-rhizobia. FEMS Microbiol Ecol 79:487–503

    Article  CAS  PubMed  Google Scholar 

  • Moulin L, James EK, Klonowska A, de Faria SM, Simon MF (2015) Phylogeny, diversity, geographical distribution, and host range of legume-nodulating betaproteobacteria: what is the role of plant taxonomy? In: de Bruijn F (ed) Biological nitrogen fixation, Wiley, Hoboken, vol 1

  • Parker MA, Wurtz A, Paynter Q (2007) Nodule symbiosis of invasive Mimosa pigra in Australia and in ancestral habitats: a comparative analysis. Biol Invasions 9:127–138

    Article  Google Scholar 

  • Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial associations with legumes. Crit Rev Plant Sci 34:17–42

    Article  Google Scholar 

  • Platero R, James EK, Rios C, Iriarte A, Sandes L, Zabaleta M, Battistoni F, Fabiano E (2016) Novel Cupriavidus strains isolated from root nodules of native Uruguayan Mimosa species. Appl Environ Microbiol 82:3150–3164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pons TL, Perreijn K, van Kessel C, Werger MJA (2007) Symbiotic nitrogen fixation in a tropical rainforest: 15N natural abundance measurements supported by experimental isotope enrichment. New Phytol 173:154–167

    Article  CAS  PubMed  Google Scholar 

  • Quirino BF, Pappas GJ, Tagliaferro AC, Collevatti RG, Neto EL, da Silva MR, Bustamante MMC, Krüger RH (2009) Molecular phylogenetic diversity of bacteria associated with soil of the savanna-like Cerrado vegetation. Microbiol Res 164:59–70

    Article  CAS  PubMed  Google Scholar 

  • Reis Junior FB, Simon MF, Gross E, Boddey RM, Elliott GN, Neto NE, Loureiro MF, Queiroz LP, Scotti MR, Chen WW, Norén A, Rubio MC, Faria SM, Bontemps C, Goi SR, Young JPW, Sprent JI, James EK (2010) Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 186:934–946

    Article  Google Scholar 

  • Robledo M, García-Trigueros C, Rivera LP, Manyani H, Mateos PF, Meguías M (2010) El viaje de Rhizobium hacia una simbiosis eficiente. In: Guijo MM, Palma RR, MJD M, MJD I, García EG, PFM G, Barrios ML, Gonzáles BR, EJB G (eds) Fundamentos y aplicaciones agroambientales de las interaciones beneficiosas plantas-microorganismos. SEFIN, Spain, pp 141–170

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Simon MF, Proença C (2000) Phtytogeografic patterns of Mimosa (Mimosoideae, Leguminosae) in the Cerrado biome of Brazil: an indicator genus of high-altitude centers of endemism? Biol Conserv 96:279–296

    Article  Google Scholar 

  • Simon MF, Hughes CE, Harris AS (2010) Four new species of Mimosa (Leguminosae) from the central highlands of Brazil. Syst Bot 35:277–288

    Article  Google Scholar 

  • Simon MF, Grether R, Queiroz LP, Sarkinen TE, Dutra VF, Hughes CE (2011) The evolutionary history of Mimosa (Leguminosae): towards a phylogeny of the sensitive plants. Am J Bot 98:1201–1221

    Article  PubMed  Google Scholar 

  • Sprent JI (2009) Legume nodulation. A global perspective. Wiley-Blackwell, Chichester

    Book  Google Scholar 

  • Sprent JI, Ardley JA, James EK (2017) Biogeography of nodulated legumes and their nitrogen fixing symbionts. New Phytol 215:40–56

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stopnisek N, Bodenhausen N, Frey B, Fierer N, Eberl L, Weisskopf L (2014) Genus-wide acid tolerance accounts for the biogeographical distribution of soil Burkholderia populations. Environ Microbio 16:1503–1512

    Article  CAS  Google Scholar 

  • Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonca-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266

    Article  PubMed  Google Scholar 

  • Thrall PH, Laine A-L, Broadhurst LM, Bagnall DJ, Brockwell J (2011) Symbiotic effectiveness of rhizobial mutualists varies in interactions with native Australian legume genera. PLoS One 6:1–11

    Article  Google Scholar 

  • Vandamme P, Goris J, Chen WM, Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 25:507–512

    Article  PubMed  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of root-nodule bacteria. Oxford: Blackwell Scientific (International Biological Programme handbook, 15)

  • Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Phil Trans R Soc B 368:20130119

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang D, Yang S, Tang F, Zhu H (2012) Symbiosis specificity in the legume-rhizobial mutualism. Cell Microbiol 14:334–342

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank managers and authorities for permission to collect in areas under their care, and Aécio Amaral, Alessandra Fidelis, Lucas Rolim, Clodoaldo Alves de Souza, for field and laboratory assistance. Authors also acknowledge Ieda de Carvalho Mendes and Marco Pessoa Filho (Embrapa Cerrados) for revising and giving suggestions on the manuscript. RCP was supported by a Master’s scholarship from the Brazilian National Council for Scientific and Technological Development (CNPq), EKJ was funded by the CAPES/CNPq Ciência sem Fronteiras program, and MFS was supported by a CNPq productivity fellowship. This research was partially financed by Embrapa (02.13.08.001.00.00) and INCT - Plant-Growth Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (CNPq 465133/2014-4, Fundação Araucária-STI, CAPES).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Fábio Bueno dos Reis Junior or Marcelo Fragomeni Simon.

Additional information

Responsible Editor: Katharina Pawlowski

Electronic supplementary material

ESM 1

(PDF 326 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Castro Pires, R., dos Reis Junior, F.B., Zilli, J.E. et al. Soil characteristics determine the rhizobia in association with different species of Mimosa in central Brazil. Plant Soil 423, 411–428 (2018). https://doi.org/10.1007/s11104-017-3521-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3521-5

Keywords

Navigation