Abstract
Root nodules have intrigued mankind ever since their role in the maintenance of soil fertility has been known. The earlier school of thought amongst microbiologists and agronomists was that root nodules are highly specialised structures rich in leghaemoglobin, which house the diazotrophic bacterium Rhizobium, whose primary role was to fix atmospheric nitrogen in association with the host plant. But several path-breaking discoveries over the past few decades have thrown light on the plethora of bacterial occupants of the root nodules and their possible role in nodulation and N fixation besides several other beneficial roles. Recent technological advances in bacterial taxonomy and microbial ecology have unearthed a wide range of microbial nodule occupants, some of which have been encompassed under the classical umbrella of rhizobia, purely based on their ability to nodulate the host and fix atmospheric nitrogen, while other closely or even distantly related bacterial genera devoid of the ability to nodulate and fix nitrogen in nodules are often referred to as endophytes or simply nodule inhabitants. This chapter attempts to capture the existing knowledge on the root nodule associated bacteria both rhizobial and non-rhizobial and their possible roles in sustaining plant growth.
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References
Allen ON, Allen EK (1981) The Leguminosae: a source book of characteristics, uses and nodulation. University of Wisconsin Press/Macmillan Publishing, Madison/London
Ardley JK, Parker MA, De Meyer SE, Trengove RD, O’Hara GW, Reeve WG, Yates RY, Dilworth MJ, Willems A, Howieson JG (2012) Microvirga lupini sp. nov., Microvirga lotononidis sp. nov., and Microvirga zambiensis sp. nov. are alphaproteobacterial root nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int J Syst Evol Microbiol 62:2579–2588
Bai YM, Daoust F, Smith DL, Driscoll BT (2002) Isolation of plant-growth-promoting Bacillus strains from soybean root nodules. Can J Microbiol 48:230–238
Basu PS, Ghosh AC (1998) Indole acetic acid and its metabolism in root nodules of a monocotyledonous tree Roystonea regia. Curr Microbiol 37:137–140
Bautista VV, Monsalud RG, Yokota A (2010) Devosia yakushimensis sp. nov., isolated from root nodules of Pueraria lobata (Willd.) Ohwi. Int J Syst Evol Microbiol 60:627–632
Benhizia Y, Benhizia H, Benguedouar A, Muresu R, Giacomini A, Squartini A (2004) Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol 27(4):462–468
Bontemps C, Elliot GN, Simon MF, Fabio B, Gross E, Lawton RC, Neto NE, Da Fa M, De FaLouriero TM, De Farion SM, Spernt JI, James EK, Young PW (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52
Bowen GJ, Beerling DJ, Koch PL, Zachos JC, Quattlebaum T (2004) A humid climate state during the Palaeocene/Eocene thermal maximum. Nature 432:495–499
Brewin NJ (2004) Plant cell wall remodelling in the Rhizobium-legume symbiosis. CRC Crit Rev Plant Sci 23:293–326
Chen WX, Yan GH, Li LJ (1988) Numerical taxonomic study of fast-growing soybean rhizobial and proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Bacteriol 38:392–397
Chen WM, Laevens S, Lee TM, Coenye T, Vos PD, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735
Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by β proteobacteria is widespread in nature. J Bacteriol 185:7266–7272
Chen WM, James EK, Coenye T, Chou JH, Edmundo B, de Faria SM, Elliott GN, Sheu SY, Sprent JI, Peter V (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
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
Chen WM, de Faria SM, Chou JH, James EK, Elliott GN, Sprent JI, Bontemps C, Young JPW, Vandamme P (2008) Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 58:2174–2179
Chou YJ, Elliott GN, James EK, Lin KY, Chou JH, Sheu SY, Sheu DS, Sprent JI, Chen WM (2007) Labrys neptuniae sp. nov., isolated from root nodules of the aquatic legume Neptunia oleracea. Int J Syst Evol Microbiol 57:577–581
Coenye T, Laevens S, Willems A, Ohlen M, Hannant W, Govan JRW, Gillis M, Falsen E, Vandamme P (2001) Burkholderia fungorum sp. nov. and Burkholderia caledonica sp. nov., two new species isolated from the environment, animals and human clinical samples. Int J Syst Evol Microbiol 51:1099–1107
da Silva K, Florentino LA, da Silva KB, de Brandt E, Vandammec V, de Souza Moreira FM (2012) Cupriavidus necator isolates are able to fix nitrogen in symbiosis with different legume species. Syst Appl Microbiol 35:175–182
Dashti N, Khanafer M, El-Nemr IN, Sorkhoh N, Radwan AS (2009) The potential of oil-utilizing bacterial consortia associated with legume root nodules for cleaning oily soils. Chemosphere 74:1354–1359
De Lajudie P, Willems A, Pot B, Dewettinck D, Maestrojuan G, Neyra M, Collins MD, Dreyfus B, Kersters K, Gillis M (1994) Polyphasic taxonomy of rhizobia: emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov., and Sinorhizobium teranga sp. nov. Int J Syst Bacteriol 44:715–733
De Lajudie P, Willems A, Nick G, Mohamed SH, Torck U, Coopman R, Filali-Maltouf A, Kersters K, Dreyfus B, Lindstrom K, Gillis M (1999) Agrobacterium bv. 1 strains isolated from nodules of tropical legumes. Syst Appl Microbiol 22:119–132
Garu G, Yates RJ, Deiana P, Howieson JG (2009) Novel strains of nodulating Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils. Soil Biol Biochem 41:125–134
Han SZ, Wang ET, Chen WX (2005) Diverse bacteria isolated from root nodules of Phaseolus vulgaris and species within the genera Campylotropis and Cassia grown in China. Syst Appl Microbiol 28:265–276
Hung PQ, Kumar SM, Govindsamy V, Annapurna K (2007) Isolation and characterization of endophytic bacteria from wild and cultivated soybean varieties. Biol Fertil Soils 44:155–162
Ibánẽz F, Angelini J, María TT, Tonelli L, Fabra A (2009) Endophytic occupation of peanut root nodules by opportunistic Gammaproteobacteria. Syst Appl Microbiol 32:49–55
Jourand P, Giraud E, Bena G, Sy A, Willems A, Gillis M, Dreyfus B, de Lajudie P (2004) Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule forming and nitrogen-fixing bacteria. Int J Syst Evol Microbiol 54:2269–2273
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
Lavin M, Pennington RT, Klitgaard BB, Sprent JI, de Lima HC, Gasson PE (2001) The Dalbergioid legume (Fabaceae): delimitation of a pantropical monophyletic clade. Am J Bot 88:503–533
Lazdunski AM, Ventre I, Sturgis JN (2004) Regulatory circuits and communication in Gram-negative bacteria. Nat Rev Microbiol 2:581–592
Li JH, Wang ET, Chen WF, Chen WX (2008) Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Soil Biol Biochem 40:238–246
Lin DX, Wang ET, Tang H, Han TX, He YR, Guan SH, Chen WX (2008) Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea. Int J Syst Evol Microbiol 58:1409–1413
Lloret L, Ormeño-Orrillo E, Rincón R, Martinez-Romero J, Rogel-Hernandez MA, Martinez-Romero E (2007) Ensifer mexicanus sp. nov. a new species nodulating Acacia angustissima (Mill.) Kuntze in Mexico. Syst Appl Microbiol 30:280–290
Lortet G, Mear N, Lorquin J, Dreyfus B, de Lajudie P, Rosenberg C, Boivin C (1996) Nod factor thin-layer chromatography profiling as a tool to characterize symbiotic specificity of rhizobial strains: application to Sinorhizobium saheli, S. teranga and Rhizobium sp. strains isolated from Acacia and Sesbania. Mol Plant-Microbe Interact 9:736–747
Mantelin S, Fischer-Le Saux M, Zakhia F, BenaG BS, Jeder H, de Lajudie P, Cleyet-Marel J-C (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 brassicacearum sp. nov. Int J Syst Evol Microbiol 56:827–839
Merabet C, Martens M, Mahdhi M, Zakhia F, Sy A, Coopman R, Bekki A, Mars M, Willems A, de Lajudie P (2010) Multilocus sequence analysis of root nodule isolates from Lotus arabicus (Senegal), Lotus creticus, Argyrolobium uniflorum and Medicago sativa (Tunisia) and description of Ensifer numidicus sp. nov. and Ensifer garamanticus sp. nov. Int J Syst Evol Microbiol 60:664–674
Mhamdi R, Laguerre G, Aouani ME, Mars M, Amarger N (2002) Different species and symbiotic genotypes of field rhizobia can nodulate Phaseolus vulgaris in Tunisian soil. FEMS Microbiol Ecol 41:77–84
Mishra PK, Mishra S, Selvakumar G, Kundu S, Gupta HS (2008) Enhanced soybean (Glycine max L.) plant growth and nodulation by Bradyrhizobium japonicum SB1 in presence of Bacillus thuringiensis-KR1. Acta Agric Scand Sect B-Plant Soil Sci 59:189–196
Mishra PK, Mishra S, Selvakumar G, Kundu S, Bisht JK, Gupta HS (2009) Coinoculation of Bacillus thuringeinsis-KR1 with enhances plant growth and nodulation of Pea (Pisum sativum L.) and Lentil (Lens culinaris L.). World J Microbiol Biotechnol 25:753–761
Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the β subclass of Proteobacteria. Nature 411:948–950
Mrabet M, Mnasri B, Romdhane SB, ĺe Laguerre G, Aouani ME, Mhamdi R (2006) Agrobacterium strains isolated from root nodules of common bean specifically reduce nodulation by Rhizobium gallicum. FEMS Microbiol Ecol 56:304–309
Muresu R, Maddau G, Delogu G, Cappuccinelli P, Squartini A (2010) Bacteria colonizing root nodules of wild legumes exhibit virulence-associated properties of mammalian pathogens. Antonie van Leeuwenhoek 97:143–153
Nick G, de Lajudie P, Eardly BD, Suomalainen S, Paulin L, Zhang X, Gillis M, Lindström K (1999) Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int J Syst Bacteriol 49:1359–1368
Okubo T, Ikeda S, Kaneko T, Eda S, Mitsuyi H, Sato S, Tabata S, Minamisawa K (2009) Nodulation-dependent communities of culturable soybean endophytes from stems of field grown endophytes. Microb Environ 24:253–258
Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T (2010) Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fertil Soils 46:807–816
Pandey P, Maheshwari DK (2007) Two-species microbial consortium for growth promotion of Cajanus cajan. Curr Sci 92:1137–1142
Rajendran G, Patel MH, Joshi SJ (2012) Isolation and characterization of nodule-associated Exiguobacterium sp. from the root nodules of Fenugreek (Trigonella foenum-graecum) and their possible role in plant growth promotion. Int J Microbiol. doi: 10.1155/2012/693982
Remans R, Beebe S, Blair M, Manrique G, Tovar E, Rao I, Croonenborghs A, Gutierrez RT, El-Howeity M, Michiels J, Vanderleyden J (2008) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161
Rivas R, Velázquez E, Willems A, Vizcaino N, Subbarao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E (2002) A new species of Devosia that forms a unique nitrogen-fixing root nodule symbiosis with the aquatic legume Neptunia natans (L.F.) Druce. Appl Environ Microbiol 68:5217–5222
Rome S, Fernandez MP, Brunel B, Normand P, Cleyet-Marel JC (1996) Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int J Syst Bacteriol 46:972–980
Scheublin TR, Ridgway KP, Young JP, van der Heijden MG (2004) Non legumes, legumes and root nodules harbour different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246
Schulz B, Boyle C (2006) What are endophytes. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes, vol 9. Springer, Berlin
Selvakumar G, Kundu S, Gupta AD, Shouche YS, Gupta HS (2008) Isolation and characterization of nonrhizobial plant growth promoting bacteria from nodules of Kudzu (Pueraria thunbergiana) and their effect on wheat seedling growth. Curr Microbiol 56:134–139
Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, James EK, Sprent JI, Young PW, Chen WM (2012) Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int J Syst Evol Microbiol 62:2272–2278
Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective of the occurrence of nodulation. New Phytol 171:11–25
Sprent JI, James EK (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575–581
Stajković O, De Meyer S, Miličić B, Willems A, Delić D (2009) Isolation and characterization of endophytic non-rhizobial bacteria from root nodules of alfalfa (Medicago sativa L.). Bot Serbica 33:107–114
Sturz AV, Christie BR, Matheson BG, Nowak J (1997) Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol Fertil Soils 25:13–19
Sy A, Giraud E, Jourand P, Garcia N, Willems A, DeLajudie P, Prin Y, Neyra 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
Talbott HJ, Kenworthy WJ, Legg JO (1982) Field comparison of the 15N and difference methods of measuring nitrogen fixation. Agron J 74:799–804
Tariq M, Hameed S, Yasmeen T, Amanat A (2012) Non-rhizobial bacteria for improved nodulation and grain yield of mung bean [Vigna radiata (L.) Wilczek]. Afr J Biotechnol 11:15012–15019
Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171
Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludena D, Mateos PF, Molina EM, Velazquez E (2005) Nodulation of Lupinus albus by strains of Ochrobactrum lupine sp. nov. Appl Environ Microbiol 71:1318–1327
Trujillo ME, Alonso-Vega P, Rodríguez R, Carro L, Cerda E, Alonso P, Martínez-Molina E (2010) The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J 4:1265–1281
Valverde A, Velazquez E, Gutierrez C, Cervantes E, Ventosa A, Igual JM (2003) Herbaspirillum lusitanum sp. nov., a novel nitrogen fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 53:1979–1983
Valverde A, Velazquez E, Fernandez-Santos F, Vizcaino N, Rivas R, Mateos PF, Molina EM, Igual JM, Willems A (2005) Phyllobacterium trifolii sp nov. nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol 55:1985–1989
Van Berkum P, Eardly BD (2002) The aquatic budding bacterium Blastobacter denitrificans is a nitrogen fixing symbiont of Aeschynomene indica. Appl Environ Microbiol 68:1132–1136
Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite application. Annu Rev Plant Physiol Plant Mol Biol 42:373–390
Vandamme P, Goris J, Chen WM, de 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
Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, Mahenthiralingam E, Speert DP, Dowson D, Vandamme P (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59:102–111
Wang ET, Tan ZY, Willems A, Fernández-López M, Reinhold-Hurek B, Martínez-Romero E (2002) Sinorhizobium morelense sp. nov., a Leucaena leucocephala associated bacterium that is highly resistant to multiple antibiotics. Int J Syst Evol Microbiol 52(5):1687–1693
Wang ET, Tan ZY, Guo XW, Rodríguez-Duran R, Boll G, Martínez-Romero E (2006a) Diverse endophytic bacteria isolated from a leguminous tree Conzattia multixora grown in Mexico. Arch Microbiol 186:251–259
Wang LL, Wang ET, Liu J, Li Y, Chen WX (2006b) Endophytic occupation of root nodules and roots of Melilotus dentatus by Agrobacterium tumefaciens. Microb Ecol 52:436–443
Wei GH, Wang ET, Tan ZY, Zhu ME, Chen WX (2002) Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol 52:2231–2239
Willems A, Fernández-López M, Muñoz E, Goris J, Martínez-Romero E, Toro N, Gillis M (2003) Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Cassida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an Opinion. Int J Syst Evol Microbiol 53:1207–1217
Zakhia F, de Lajudie P (2001) Taxonomy of rhizobia. Agronomie 21:569–576
Zakhia F, Jeder H, Willems A, Gillis M, Dreyfus B, de Lajudie P (2006) Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nif H like gene within the genera Microbacterium and Starkeya. Microb Ecol 51:375–393
Zurdo-Piñeiro JL, Rivas R, Trujillo ME, Vizcaíno N, Carrasco JA, Chamber M, Palomares A, Mateos PF, Martínez-Molina E, Velázquez E (2007) Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain. Int J Syst Evol Microbiol 57:784–788
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Selvakumar, G., Panneerselvam, P., Ganeshamurthy, A.N. (2013). Legume Root Nodule Associated Bacteria. In: Arora, N. (eds) Plant Microbe Symbiosis: Fundamentals and Advances. Springer, New Delhi. https://doi.org/10.1007/978-81-322-1287-4_8
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