Skip to main content
Log in

Bradyrhizobium campsiandrae sp. nov., a nitrogen-fixing bacterial strain isolated from a native leguminous tree from the Amazon adapted to flooded conditions

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The nitrogen-fixing bacterial strain UFLA 01-1174T was isolated from nodules of Campsiandra laurilifolia Benth. originating from the Amazon region, Brazil. Its taxonomic position was defined using a polyphasic approach. Analysis of the 16S rRNA gene placed the strain in the Bradyrhizobium genus, the closest species being B. guangdongense CCBAU 51649T and B. guangzhouense CCBAU 51670T, both with 99.8% similarity. Multilocus sequence analysis (MLSA) of recA, gyrB, glnII, rpoB, atpD, and dnaK indicated that UFLA 01-1174is a new species, most closely related to B. stylosanthis BR 446T (94.4%) and B. manausense BR 3351T (93.7%). Average nucleotide identity (ANI) differentiated UFLA 01-1174T from the closest species with values lower than 90%. The G + C content in the DNA of UFLA 01-1174is 63.6 mol%. Based on this data, we conclude that the strain represents a new species. The name proposed is Bradyrhizobium campsiandrae, with UFLA 01-1174T (= INPA 394BT = LMG 10099T) as type strain.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Andrews M, De Meyer S, James EK, Stepkowski T, Hodge S, Simon MF, Young JPW (2018) Horizontal transfer of symbiosis genes within and between rhizobial genera: occurrence and importance. Genes (Basel) 9(7):321

    Google Scholar 

  • Avontuur JR, Palmer M, Beukes CW, Chan WY, Cetzee MPA, Blom J, Stepkowski T, Kyrpides NC, Woyke T, Shapiro N, Whitmam WB, Venter SN, Steenkamp T (2019) Genome-informed Bradyrhizobium taxonomy: where to from here? Syst Appl Microbiol 42:427–439

    PubMed  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beuker CW, Stepkowski T, Venter SN, Cłapa T, Phalane FL, le Roux MM, Steenkamp ET (2016) Crotalarieae and Genisteae of the South African great escarpment are nodulated by novel Bradyrhizobium species with unique and diverse symbiotic loci. Mol Phylogenet Evol 100:206–218

    Google Scholar 

  • Castellanos C, Lewis GP (2012) Leguminosas colombianas de la subfamilia Caesalpinioideae presentes en El Herbário del Real Jardín Botánico de Kew, Reino Unido. Revista de la Academia Colombiana de Ciências Exactas, Físicas y Naturales 36:141–192

    Google Scholar 

  • Chahboune R, Carro L, Peix A, Barrijal S, Velázquez E, Bedmar EJ (2011) Bradyrhizobium cytisi sp. nov., isolated from effective nodules of Cytisus villosus. Int Int J Syst Evol Microbiol 61:2922–2927

    PubMed  Google Scholar 

  • Chan JZM, Halachev MR, Loman NJ, Constantinidou C, Pallen MJ (2012) Defining bacterial species in the genomic era: insights from the genus Acinetobacter. BMC Microbiol 12:302

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ciufo S, Kannan S, Sharma S, Badretdin A, Clark K, Turner S, Brover S, Schoch CL, Kimchi A, DiCuccio M (2018) Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI. Int J Syst Evol Microbiol 68:2386–2392

    PubMed  PubMed Central  Google Scholar 

  • Corrêa MP (1926) Dicionário das plantas úteis do Brasil e das exóticas cultivadas. Rio de Janeiro Ministério da agricultura, Indústria e Comércio 1:24

    Google Scholar 

  • 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

    Google Scholar 

  • Costa EM, Guimarães AA, de Carvalho TS, Rodrigues TL, Ribeiro PRA, Lebbe L, Willems A, Moreira FMS (2018) Bradyrhizobium forestalis sp nov., an efficient nitrogen-fixing bacterium isolated from nodules of forest legume species in the Amazon. Arch Microbiol 200:743–752

    Google Scholar 

  • Darling AE, Mau B, Perna NT (2010) Progressive Mauve: multiple alignment of genomes with gene flux and rearrangement. PLoS ONE 5:e11147. https://doi.org/10.1371/journal.pone.0011147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Faria SM, Lewis GP, Sprent JI, Sutherland JM (1989) Occurrence of nodulation in the Leguminosae. New Phytol 111:607–619

    Google Scholar 

  • De Lajudie PM, Andrews M, Ardley J, Eardly B, Jumas-Bilak E, Kuzmanovic N, Lassale F, Lindström K, Mhamdi R, Martínez-Romero E, Moulin L, Mousavi SA, Nesme X, Peix A, Putawska J, Steenkamp E, Stepkowski T, Tian CF, Vinuesa P, Wei G, Willems A, Zilli J, Young P (2019) Minimal standards for the description of new genera and species of rhizobia and agrobacteria. Int J Syst Evol Microbiol 69(7):1852–1863

    PubMed  Google Scholar 

  • Durán D, Rey L, Sanchez-Cañizares C, Jorrin B, Imperial J, Ruiz-Argüeso T (2013) Biodiversity of slow-growing Rhizobia: the genus Bradyrhizobium. CRC Press, Boca Raton

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    CAS  PubMed  Google Scholar 

  • Florentino LA, Sousa PM, Silva JS, Silva KB, Moreira FMS (2010) Diversity and efficiency of Bradyrhizobium strains isolated from soil samples collected from around Sesbania virgata roots using cowpea as trap species. Rev Bras Cienc Solo 34:1113–1123

    CAS  Google Scholar 

  • Fred EB, Waksman SA (1928) Laboratory manual of general microbiology with special reference to the microorganisms of the soil. McGraw-Hill Book, New York, p 145

    Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    CAS  PubMed  Google Scholar 

  • Herrera A, Tezara W, Rengifo E, Flores S (2008) Changes with seasonal flooding in sap flow of the tropical flood-tolerant tree species, Campsiandra laurilifolia. Trees 22(4):551–558

    Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197

    PubMed  Google Scholar 

  • Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Micr 64:346–351

    CAS  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005) Genomic insights that advance the species definition for prokaryotes. PNAS 7:2567–2572

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) Mega 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuykendall LD, Saxena B, Devine TE, Udell SE (1992) Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can J Microbiol 38:501–505

    CAS  Google Scholar 

  • Macbride JF (1943) Flora of Peru. Field museum of natural history. Bot Ser 13(1):204

    Google Scholar 

  • MAPA (Ministério da Agricultura, Pecuária e Abastecimento) (2011) Instrução normative SDA n°13

  • Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A (2018) MUMmer 4: a fast versatile genome alignment system. PLoS Comput Biol 14:e1005944

    PubMed  PubMed Central  Google Scholar 

  • Moreira FMS (1997) Nursery growth and nodulation of forty-nine woody legume species native from Amazonia. Rev bras Ci Sol 21:581–590

    Google Scholar 

  • Moreira FMS, Silva MF, Faria SM (1992) Occurrence of nodulation in legume species in the Amazon region of Brazil. New Phytol 121:563–570

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ormeño-Orrillo E, Servín-Garcidueñas LE, Rogel MA, González V, Peralta H, Mora J, Martínez-Romero J, Martínez-Romer E (2015) Taxonomy of rhizobia and agrobacteria from the Rhizobiaceae family in light of genomics. Syst Appl Microbiol 38(4):287–291

    PubMed  Google Scholar 

  • Parker MA (2015) The spread of Bradyrhizobium Lineages across host legume clades: from Abarema to Zygia. Microb Ecol 69:630–640

    PubMed  Google Scholar 

  • Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells and metagenomes. Genomes Res 25:1043–1055

    CAS  Google Scholar 

  • Ramírez-Bahena MH, Chahboune R, Peix A, Velázquez E (2012) Reclassification of Agromonas oligotrophica into genus Bradyrhizobium as Bradyrhizobium oligotrophicum comb. nov. Int J Syst Evol Microbiol 63:1013–1016

    PubMed  Google Scholar 

  • Remigi P, Zhu J, Young PW, Masson-Boivin C (2016) Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24(1):63–75

    CAS  PubMed  Google Scholar 

  • Rengifo E, Tezara W, Herrera A (2005) Water relations, chlorophyll α fluorescence, and contents of saccharides in tree species of a tropical forest in response to flood. Photosynthetica 43(2):203–210

    CAS  Google Scholar 

  • Ribeiro PRA, Santos JV, Costa EM, Lebbe L, Louzada MO, Guimarães AA, Assis ES, Willems A, Moreira FMS (2015) Symbiotic efficiency and genetic diversity of soybean bradyrhizobia in Brazilian soils. Agr Ecosyst Environ 212:85–93

    Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas R, García-Fraile P, Velázquez E (2009a) Taxonomy of bacteria nodulating legumes. Microbiol Insights 2:3137

    Google Scholar 

  • Rivas R, Martens M, de Lajudie P, Willems A (2009b) Multilocus sequence analysis of the genus Bradyrhizobium. Syst Appl Microbiol 32:101–110

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Silva FV, De Meyer SE, Simões-Araújo JL, Barbé TC, Xavier GR, O’Hara G, Ardley JK, Rumjanek NG, Willems A, Zilli JE (2014) Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazon rainforest soils. Int J Syst Evol Microbiol 64:2358–2363

    CAS  PubMed  Google Scholar 

  • Sprent JI, Parsons R (2000) Nitrogen fixation in legume and non-legume trees. Field Crop Res 65:183–196

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Stergios B (1996) Contributions to South American Caesalpiniaceae. II. A Taxonomic Update of Campsiandra (Caesalpinieae) https://www.jstor.org/stable/3392055

  • 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

    CAS  PubMed  Google Scholar 

  • Ulibarri EA (2008) Los géneros de Caesalpinioideae (Leguminosae) presentes en Sudamérica. Darwiniana 46(1):69–163

    Google Scholar 

  • Vieira DS, Oliveira MLR, Gama JRV, Machado ELM, Görgens EB, Lafetá BO, Garcia JS (2017) Phytosociology of a natural fragment of the floodplain forest in the lower Tapajós River, Brazil. Bosque 38:357–369

    Google Scholar 

  • Willems A, Coopman R, Gillis M (2001) Phylogenetic and DNA-DNA hybridization analyses of Bradyrhizobium species. Int J Syst Evol Microbiol 51:111–117

    CAS  PubMed  Google Scholar 

  • Xu LM, Ge C, Cui Z, Li J, Fan H (1995) Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 45:706–711

    CAS  PubMed  Google Scholar 

  • Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286

    CAS  PubMed  Google Scholar 

  • Zhang YM, Tian CF, Sui XH, Chen WF, Chen WX (2012) Robust markers phylogeny and taxonomy of rhizobia. PLoS ONE 7:e44936

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (CAPES/PROEX AUXPE 593/2018), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Process: 304527/2016-5; Process: 431504/2016-4), and the Fundação de Amparo e Pesquisa de Minas Gerais (Fapemig) (PACCSS/PPGCS—2009–2012) for financial support and for granting scholarships. This research is associated with the Brazilian Instituto Nacional de Ciência e Tecnologia Biodiversidade do Solo (Soil Biodiversity/INCT-CNPq).The authors would also like to thank the Fapemig, Capes, CNPq and Finep (Financiadora de Estudos e Projetos)for maintaining the electron microscopy laboratory and Bruna Ortiz Lopez for the great picture of the strain of this study (Fig S2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fatima Maria de Souza Moreira.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cabral Michel, D., Martins da Costa, E., Azarias Guimarães, A. et al. Bradyrhizobium campsiandrae sp. nov., a nitrogen-fixing bacterial strain isolated from a native leguminous tree from the Amazon adapted to flooded conditions. Arch Microbiol 203, 233–240 (2021). https://doi.org/10.1007/s00203-020-02022-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-020-02022-7

Keywords

Navigation