Soil characteristics determine the rhizobia in association with different species of Mimosa in central Brazil
- 547 Downloads
Background and aims
To evaluate the influence of soil type on the symbiosis between Mimosa spp. and rhizobia.
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.
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.
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.
KeywordsBiological nitrogen fixation Cerrado Host-specificity Nodulation Rhizobia β-rhizobia
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).
- 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 66:1–7CrossRefGoogle Scholar
- Barneby RC (1991) Sensitivae Censitae: a description of the genus Mimosa Linnaeus (Mimosaceae) in the new world. Mem N Y Bot Gard 65:1–835Google 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, 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 209:319–333CrossRefPubMedGoogle 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 71:7461–7471CrossRefPubMedPubMedCentralGoogle 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 57:1055–1059CrossRefPubMedGoogle 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: fiw108Google 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 29:609–619CrossRefPubMedGoogle 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 173:168–180CrossRefPubMedGoogle Scholar
- Embrapa (1997) Manual de métodos de análise de solo. 2ª ed. Centro Nacional de Pesquisa de Solos, Rio de Janeiro, p 212Google Scholar
- 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 66:1303–1314Google Scholar
- Fred EB, Waskman SA (1928) Yeast extract-manitol agar. Laboratory manual of general microbiology. McGraw-Hill, New York, p 145Google 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 112:179–196CrossRefGoogle 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 24:1276–1288CrossRefPubMedGoogle Scholar
- Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95 ⁄ 98 ⁄ NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
- Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. California agricultural experimental station. Circ. n.347Google 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 81:618–635CrossRefPubMedGoogle 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 393:123–135Google Scholar
- 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 91:1–17CrossRefPubMedGoogle 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 16:2099–2111CrossRefPubMedGoogle 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.Google Scholar
- 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 79:487–503CrossRefPubMedGoogle 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 1Google 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 186:934–946CrossRefGoogle 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 141–170Google 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 5:429CrossRefPubMedPubMedCentralGoogle Scholar
- Vincent JM (1970) A manual for the practical study of root-nodule bacteria. Oxford: Blackwell Scientific (International Biological Programme handbook, 15)Google Scholar