Phenotypic and genotypic diversity of root nodule bacteria from wild Lathyrus and Vicia species in Gaziantep, Turkey.
Rhizobium
16S rRNA
Diversity
Nodulation
Wild legumes
Journal
Folia microbiologica
ISSN: 1874-9356
Titre abrégé: Folia Microbiol (Praha)
Pays: United States
ID NLM: 0376757
Informations de publication
Date de publication:
25 Mar 2024
25 Mar 2024
Historique:
received:
18
09
2023
accepted:
08
03
2024
medline:
25
3
2024
pubmed:
25
3
2024
entrez:
25
3
2024
Statut:
aheadofprint
Résumé
This study identified the phenotypic and genotypic characteristics of the bacteria that nodulate wild Lathyrus and Vicia species natural distribution in the Gaziantep province of Turkey. Principle component analysis of phenotypic features revealed that rhizobial isolates were highly resistant to stress factors such as high salt, pH and temperature. They were found to be highly sensitive to the concentrations (mg/mL) of the antibiotics neomycin 10, kanamycin, and tetracycline 5, as well as the heavy metals Ni 10, and Cu 10, and 5. As a result of REP-PCR analysis, it was determined that the rhizobial isolates were quite diverse, and 5 main groups and many subgroups being found. All of the isolates nodulating wild Vicia species were found to be related to Rhizobium sp., and these isolates were found to be in Clades II, III, IV, and V of the phylogenetic tree based on 16S rRNA. The isolates that nodulated wild Lathyrus species were in Clades I, II, IV, V, VI, VII, and VIII, and they were closely related to Rhizobium leguminasorum, Rhizobium sp., Phyllobacterium sp., Serratia sp., and Pseudomonas sp. According to the genetic analyses, the isolates could not be classified at the species level, the similarity ratio was low, they formed a distinct group that was supported by strong bootstrap values in the phylogenetic tree, and the differences discovered in the network analysis revealed the diversity among the isolates and gave important findings that these isolates may be new species.
Identifiants
pubmed: 38526677
doi: 10.1007/s12223-024-01156-1
pii: 10.1007/s12223-024-01156-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i.
Références
Adiguzel A, Ogutcu H, Baris O, Karadayi M, Gulluce M, Sahin F (2010) Isolation and characterization of rhizobium strains from wild vetch collected from high altitudes in Erzurum-Turkey. Rom Biotechnol Lett 15:5017–5024
Ahmad MH, Uddin MR, McLaughlin W (1984) Characterization of indigenous rhizobia from wild legumes. FEMS Microbiol Lett 24:197–203
doi: 10.1111/j.1574-6968.1984.tb01304.x
Alexandre A, Laranjo M, Oliveira S (2006) Natural populations of chickpea rhizobia evaluated by antibiotic resistance profiles and molecular methods. Microb Ecol 51:128–136
doi: 10.1007/s00248-005-0085-3
pubmed: 16389465
Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int J Syst Bacteriol 47:996–1006
doi: 10.1099/00207713-47-4-996
pubmed: 9336898
Ampomah OY, Huss-Danell K (2016) Genetic diversity of rhizobia nodulating native Vicia spp. in Sweden. Syst Appl Microbiol 39:203–210
doi: 10.1016/j.syapm.2016.02.002
pubmed: 26924220
Amsalu A, Assefa F, Hailemariam A (2012) Symbiotic and phenotypic characterization of rhizobium isolates of field pea (Pisum sativum L.) fabecae, from central and southern Ethiopia. Ethiop J Biol Sci 11:163–179
Aoki S, Kondo T, Prévost D, Nakata S, Kajita T, Ito M (2010) Genotypic and phenotypic diversity of rhizobia isolated from Lathyrus japonicus indigenous to Japan. Syst Appl Microbiol 33:383–397
doi: 10.1016/j.syapm.2010.07.001
pubmed: 20851546
Basbuga S, Basbuga S, Yayla F, Mahmoud AM, Can C (2021) Diversity of rhizobial and non-rhizobial bacteria nodulating wild ancestors of grain legume crop plants. Int Microbiol 24:207–218
doi: 10.1007/s10123-020-00158-6
pubmed: 33423098
Bernal G, Graham PH (2001) Diversity in the rhizobia associated with Phaseolus vulgaris L. in Ecuador, and comparisons with Mexican bean rhizobia. Can J Microbiol 47:526–534
doi: 10.1139/w01-037
pubmed: 11467728
Berrada H, Nouioui I, Houssaını MI, Gtarı M, Benbrahım KF (2012) Phenotypic and genotypic characterizations of rhizobia isolated from root nodules of multiple legume species native of Fez, Morocco. African J Microbiol Res 6:5314–5324
Broughton WJ, Dilworth MJ (1970) Control of leghaemoglobin synthesis in snake beans. J Biochem 125:1075–1080. https://doi.org/10.1042/bj1251075
doi: 10.1042/bj1251075
Bryant D, Moulton V (2004) Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265
doi: 10.1093/molbev/msh018
pubmed: 14660700
da Silva VB, da Silva AF, da Silva TR, dos Santos JWM, da Silva JF, de Souza AP, de Freitas ADS, Fernandes-Júnior PI (2019) Fast and efficient symbiotic gene-based duplex PCR approach for the preliminary selection of legume root nodule bacteria. Rhizosphere 10:100144. https://doi.org/10.1016/j.rhisph.2019.100144
doi: 10.1016/j.rhisph.2019.100144
Davis PH (1970) Flora of Turkey and the East Aegean Islands, vol 3. University Press, Edinburgh
de Bruijn FJ (1992) Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl Environ Microbiol 58:2180–2187
doi: 10.1128/aem.58.7.2180-2187.1992
pubmed: 1637156
pmcid: 195753
De Meyer SE, Van Hoorde K, Vekeman B, Braeckman T, Willems A (2011) Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium). Soil Biol Biochem 43:2384–2396. https://doi.org/10.1016/j.soilbio.2011.08.005
doi: 10.1016/j.soilbio.2011.08.005
Doyle JJ (1994) Phylogeny of the legume famıly: an approach to understanding the origins of nodulation. Annu Rev Ecol Syst 25:325–349
doi: 10.1146/annurev.es.25.110194.001545
Drouin P, Prévost D, Antoun H (1996) Classification of bacteria nodulating Lathyrus japonicus and Lathyrus pratensis in northern Quebec as strains of Rhizobium leguminosarum biovar viciae. Int J Syst Bacteriol 46:1016–1024
doi: 10.1099/00207713-46-4-1016
pubmed: 8863431
El-Batanony NH, Castellano-Hinojosa A, Correa-Galeote D, Bedmar EJ (2020) Phylogenetic diversity of bacterial strains from root nodules of legumes grown wild in Egypt. Biocatal Agric Biotechnol 27:101692
doi: 10.1016/j.bcab.2020.101692
El-Hilali I (2006) Rhizobium-Lupine symbiosis: micro-symbioses biodiversity and highlighting of a multi nodular infection in Lupinus luteus. Dissertation, Dr Univ Mohammed V Agdal, Rabat
Gao J-L, Turner SL, Kan FL, Wang ET, Tan ZY, Qiu YH, Gu J, Terefework Z, Young JPW, Lindström K et al (2004) Mesorhizobium septentrionale sp. nov. and Mesorhizobium temperatum sp. nov., isolated from Astragalus adsurgens growing in the northern regions of China. Int J Syst Evol Microbiol 54:2003–2012. https://doi.org/10.1099/ijs.0.02840-0
doi: 10.1099/ijs.0.02840-0
pubmed: 15545425
Germano MG, Menna P, Mostasso FL, Hungria M (2006) RFLP analysis of the rRNA operon of a Brazilian collection of bradyrhizobial strains from 33 legume species. Int J Syst Evol Microbiol 56:217–229. https://doi.org/10.1099/ijs.0.02917-0
doi: 10.1099/ijs.0.02917-0
pubmed: 16403890
Gök M, Martin P (1993) Farklı Rhizobium bakterileri ile aşılamanın soya, üçgül ve fiğde simbiyotik azot fiksasyonuna etkisi. Doğa-Tr J Agric for 17:753–761
Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martinez E, Aarons SR, Quinto C (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Can J Microbiol 40:198–207
doi: 10.1139/m94-033
Gritli T, Ellouze W, Chihaoui SA, Barhoumi F, Mhamdi R, Mnasri B (2020) Genotypic and symbiotic diversity of native rhizobia nodulating red pea (Lathyrus cicera L) in Tunisia. Syst Appl Microbiol. https://doi.org/10.1016/j.syapm.2019.126049
doi: 10.1016/j.syapm.2019.126049
pubmed: 31870686
Hamdi Y. (1997) Symbiotic biological nitrogen fixation proceedings of the training course on bio-organic farming systems for sustainable agriculture. In: Cairo- Egypt. p. 79–102
Han TX, Wang ET, Wu LJ, Chen WF, Gu JG, Gu CT, Tian CF, Chen WX (2008) Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang. China Int J Syst Evol Microbiol 58:1693–1699. https://doi.org/10.1099/ijs.0.65568-0
doi: 10.1099/ijs.0.65568-0
pubmed: 18599718
Han TX, Tian CF, Wang ET, Chen WX (2010) Associations among rhizobial chromosomal background, nod genes, and host plants based on the analysis of symbiosis of indigenous rhizobia and wild legumes native to Xinjiang. Microb Ecol 59:311–323. https://doi.org/10.1007/s00248-009-9577-x
doi: 10.1007/s00248-009-9577-x
pubmed: 19730765
Haukka K, Lindström K, Young JPW (1998) Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. Appl Environ Microbiol 64:419–426
doi: 10.1128/AEM.64.2.419-426.1998
pubmed: 9464375
pmcid: 106060
Huson DH, Bryant D (2005) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030
doi: 10.1093/molbev/msj030
pubmed: 16221896
Kalkancı N, Şimşek T (2020) Efficiency status of Gaziantep soils. Pist Res J 8:8–11
Kan FL, Chen ZY, Wang ET, Tian CF, Sui XH, Chen WX (2007) Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai-Tibet plateau and in other zones of China. Arch Microbiol 188:103–115. https://doi.org/10.1007/s00203-007-0211-3
doi: 10.1007/s00203-007-0211-3
pubmed: 17541555
Kantar F (1997) Proceeding of training course on bio-organic farming systems for sustainable agriculture. In: Cairo- Egypt. p. 270–272
Karaduman A, Çimrin K (2016) Nutrient status of Gaziantep agricultural soils and their relationships with some soil properties. KSU J Agric Nat 19:117–129
Kawaka F, Makonde H, Dida M, Opala P, Ombori O, Maingi J, Muoma J (2018) Genetic diversity of symbiotic bacteria nodulating common bean (Phaseolus vulgaris) in western Kenya. PLoS ONE 13:e0207403
doi: 10.1371/journal.pone.0207403
pubmed: 30440041
pmcid: 6237360
Kim DH, Kaashyap M, Rathore A, Das RR, Parupalli S, Upadhyaya HD, Gopalakrishnan S, Gaur PM, Singh S, Kaur J et al (2014) Phylogenetic diversity of Mesorhizobium in chickpea. J Biosci 39:513–517. https://doi.org/10.1007/s12038-014-9429-9
doi: 10.1007/s12038-014-9429-9
pubmed: 24845514
Küçük Ç, Kivanc M (2008) Preliminary characterization of Rhizobium strains isolated from chickpea nodules. African J Biotechnol 7:772–775
Küçük Ç, Kivanç M, Kinaci E (2006) Characterization of Rhizobium sp. isolated from bean. Turkish J Biol 30:127–132
Laguerre G, Mavingui P, Allard MR, Charnay MP, Louvrier P, Mazurier SI, Rigottier-Gois L, Amarger N (1996) Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: application to Rhizobium leguminosarum and its different biovars. Appl Environ Microbiol 62:2029–2036
doi: 10.1128/aem.62.6.2029-2036.1996
pubmed: 8787401
pmcid: 167981
Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147:981–993. https://doi.org/10.1099/00221287-147-4-981
doi: 10.1099/00221287-147-4-981
pubmed: 11283294
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Ltd., New York, pp 115–175
Lebrazi S, Chraibi M, Fadil M, Barkai H, Fikri-Benbrahim K (2018) Phenotypic, genotypic and symbiotic characterization of rhizobial isolates nodulating Acacia sp. in Morocco. J Pure Appl Microbiol 12:249–263
doi: 10.22207/JPAM.12.1.30
Legesse S, Assefa F (2014) Symbiotic and phenotypic characteristics of rhizobia nodulating Faba bean (Vicia faba) From Tahtay Koraro, Northwestern Zone Of Tigray Regional State, Ethiopia. Int J Technol Enhanc Emerg Eng Res 2:15–23
Lei X, Wang ET, Chen WF, Sui XH, Chen WX (2008) Diverse bacteria isolated from root nodules of wild Vicia species grown in temperate region of China. Arch Microbiol 190:657–671. https://doi.org/10.1007/s00203-008-0418-y
doi: 10.1007/s00203-008-0418-y
pubmed: 18704366
Li Y, Wang ET, Liu Y, Li X, Yu B, Ren C, Liu W, Yunzhao Li, Xie Z (2016) Rhizobium anhuiense as the predominant microsymbionts of Lathyrus maritimus along the Shandong Peninsula seashore line. Syst Appl Microbiol 39:384–390
doi: 10.1016/j.syapm.2016.07.001
pubmed: 27480059
Mahmoud MA, Mart D, Can C (2019) Phenotypic characterization of indigenous rhizobia nodulating chickpea in Turkey reveals high diversity. Legum Res 42:379–384. https://doi.org/10.18805/LR-430
doi: 10.18805/LR-430
Mantelin S, Saux MF-L, Zakhia F, Béna G, Bonneau S, Jeder H, de Lajudie PM, Cleyer Marel JC (2006) Emended description of the genus Phyllobacterium and description of four novel species associated with plant roots: Phyllobacterium bourgognense sp. nov., Phyllobacterium ifriqiyense sp. nov., Phyllobacterium leguminum sp. nov. and Phyllobacterium brassic. Int J Syst Evol Microbiol 4:827–839
doi: 10.1099/ijs.0.63911-0
Martínez-Romero E, Caballero-Mellado J (1996) Rhizobium phylogenies and bacterial genetic diversity. CRC Crit Rev Plant Sci 15:113–140. https://doi.org/10.1080/07352689609701938
doi: 10.1080/07352689609701938
Missbah El Idrissi M, Lamin H, Bouhnik O, Lamrabet M, Alami S, Jabrone Y, Bennis M, Bedmar EJ, Abdelmoumen H (2020) Characterization of Pisum sativum and Vicia faba microsymbionts in Morocco and definition of symbiovar viciae in Rhizobium acidisoli. Syst Appl Microbiol 43:126084. https://doi.org/10.1016/j.syapm.2020.126084
doi: 10.1016/j.syapm.2020.126084
pubmed: 32423773
Mohammed MA, Chernet MT, Tuji FA (2020) Phenotypic, stress tolerance, and plant growth promoting characteristics of rhizobial isolates of grass pea. Int Microbiol 23:607–618. https://doi.org/10.1007/s10123-020-00131-3
doi: 10.1007/s10123-020-00131-3
pubmed: 32495247
Moschetti G, Peluso AL, Protopapa A, Anastasio M, Pepe O, Defez R (2005) Use of nodulation pattern, stress tolerance, nodC gene amplification, RAPD-PCR and RFLP-16S rDNA analysis to discriminate genotypes of Rhizobium leguminosarum biovar viciae. Syst Appl Microbiol 28:619–631. https://doi.org/10.1016/j.syapm.2005.03.009
doi: 10.1016/j.syapm.2005.03.009
pubmed: 16156120
Mutch L, Young JPW (2004) Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol Ecol 13:2435–2444. https://doi.org/10.1111/j.1365-294X.2004.02259.x
doi: 10.1111/j.1365-294X.2004.02259.x
pubmed: 15245415
Nushair AM, Saha AK, Rahman MA, Mohanta MK, Haque MF (2017) Characterization of indigenous Rhizobium strain isolated from lentil in Rajshahi, Bangladesh. Asian J Adv Basic Sci 5:21–25
Rai R, Dash PK, Mohapatra T, Singh A (2012) Phenotypic and molecular characterization of indigenous rhizobia nodulating chickpea in India. J Exp Biol 50:340–350
Ruiz-Díez B, Fajardo S, del Rosario de Felipe M, Fernández-Pascual M, (2012) Characterization of rhizobia from legumes of agronomic interest grown in semi-arid areas of Central Spain relates genetic differences to soil properties. J Basic Microbiol 52:66–78. https://doi.org/10.1002/jobm.201100058
doi: 10.1002/jobm.201100058
pubmed: 21953333
Saïdi S, Ramírez-Bahena MH, Santillana N, Zúñiga D, Álvarez-Martínez E, Peix A, Mhamdi R, Velázquez E (2014) Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. Int J Syst Evol Microbiol 64:242–247. https://doi.org/10.1099/ijs.0.052191-0
doi: 10.1099/ijs.0.052191-0
pubmed: 24067731
Santillana N, Ramírez-Bahena MH, García-Fraile P, Velázquez E, Zúñiga D (2008) Phylogenetic diversity based on rrs, atpD, recA genes and 16S–23S intergenic sequence analyses of rhizobial strains isolated from Vicia faba and Pisum sativum in Peru. Arch Microbiol 189:239–247. https://doi.org/10.1007/s00203-007-0313-y
doi: 10.1007/s00203-007-0313-y
pubmed: 17985116
Shiraishi A, Matsushita N, Hougetsu T (2010) Nodulation in black locust by the Gammaproteobacteria Pseudomonas sp. and the Betaproteobacteria Burkholderia sp. Syst Appl Microbiol 33:269–274. https://doi.org/10.1016/j.syapm.2010.04.005.h
doi: 10.1016/j.syapm.2010.04.005.h
pubmed: 20542651
Somasegaran P, Hoben HJ (1994) Handbook for rhizobia: methods in legume-rhizobium technology. 1st ed. Springer Verlag New York, Inc
Sui X, LiLi H, EnTao W, Feng J, YiHai L, WenXin C (2009) Novel associations between rhizobial populations and legume species within the genera Lathyrus and Oxytropis grown in the temperate region of China. Sci China Ser C Life Sci 52:182–192. https://doi.org/10.1007/s11427-008-0132-7
doi: 10.1007/s11427-008-0132-7
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
doi: 10.1093/molbev/msab120
pubmed: 33892491
pmcid: 8233496
Tan A (1996) Turkey: country report to the FAO International Technical Conference on Plant Genetic Resource, Leipzig, Germany
Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277:1063–1066. https://doi.org/10.1126/science.277.5329.1063
doi: 10.1126/science.277.5329.1063
pubmed: 9262467
Tena W, Wolde-Meskel E, Degefu T, Walley F (2017) Genetic and phenotypic diversity of rhizobia nodulating chickpea (Cicer arietinum L.) in soils from southern and central Ethiopia. Can J Microbiol 63:690–707. https://doi.org/10.1139/cjm-2016-0776
doi: 10.1139/cjm-2016-0776
pubmed: 28499096
Tian CF, Wang ET, Wu LJ, Han TX, Chen WF, Gu CT, Gu JG, Chen WX (2008) Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int J Syst Evol Microbiol 58:2871–2875. https://doi.org/10.1099/ijs.0.2008/000703-0
doi: 10.1099/ijs.0.2008/000703-0
pubmed: 19060074
Zaheer A, Mirza BS, Mclean JE, Yasmin S, Shah TM, Malik KA, Mirza MS (2016) Association of plant growth-promoting Serratia spp. with the root nodules of chickpea. Res Microbiol 167:510–520. https://doi.org/10.1016/j.resmic.2016.04.001
doi: 10.1016/j.resmic.2016.04.001
pubmed: 27117242
Zahir ZA, Zafar-ul-Hye M, Sajjad S, Naveed M (2011) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for coinoculation with Rhizobium leguminosarum to improve growth, nodulation, and yield of lentil. Biol Fertil Soils 47:457–465. https://doi.org/10.1007/s00374-011-0551-7
doi: 10.1007/s00374-011-0551-7
Zhang XX, Kosier B, Priefer UB (2001) Genetic diversity of indigenous Rhizobium leguminosarum bv. viciae isolates nodulating two different host plants during soil restoration with alfalfa. Mol Ecol 10:2297–2305. https://doi.org/10.1046/j.0962-1083.2001.01364.x
doi: 10.1046/j.0962-1083.2001.01364.x
pubmed: 11555271
Zhang YJ, Zheng WT, Everall I, Young JPW, Zhang XX, Tian CF, Sui XH, Wang ET, Chen WX (2015) Rhizobium anhuiense sp. nov., isolated from effective nodules of Vicia faba and Pisum sativum. Int J Syst Evol Microbiol 65:2960–2967. https://doi.org/10.1099/ijs.0.000365
doi: 10.1099/ijs.0.000365
pubmed: 26025940
Zhang J, Shang Y, Peng S, Chen W, Wang E, de Lajudie P, Li B, Guo C, Liu C (2019) Rhizobium sophorae, Rhizobium laguerreae, and two novel Rhizobium genospecies associated with Vicia sativa L. in Northwest China. Plant Soil 442:113–126. https://doi.org/10.1007/s11104-019-04168-w
doi: 10.1007/s11104-019-04168-w
Zhang J, Li S, Wang N, Yang T, Brunel B, Andrews M, Zong X, Wang E (2022) Rhizobium sophorae is the dominant rhizobial symbiont of Vicia faba L. In North China Syst Appl Microbiol 45:126291. https://doi.org/10.1016/j.syapm.2021.126291
doi: 10.1016/j.syapm.2021.126291
pubmed: 34968802