Ensifer meliloti

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Ensifer meliloti
Sinorhizobium meliloti strain Rm1021 on TY agar.JPG
Sinorhizobium meliloti strain Rm1021 on an agar plate.
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Pseudomonadota
Class: Alphaproteobacteria
Order: Hyphomicrobiales
Family: Rhizobiaceae
Genus: Ensifer
Species:
E. meliloti
Binomial name
Ensifer meliloti
(Dangeard, 1926) Young, 2003
Type strain
ATCC 9930

CCUG 27879
CFBP 5561
CIP 107332
DSM 30135
HAMBI 2148
IAM 12611
ICMP 12623
IFO 14782
JCM 20682
LMG 6133
NBRC 14782
NCAIM B.01520
NCIMB 12075
NRRL L-45
NZP 4027
OUT 30010
USDA 1002

Contents

Biovars
  • S. m. bv. acaciae [1]
  • S. m. bv. ciceri [2] [3]
  • S. m. bv. lancerottense [4]
  • S. m. bv. medicaginis [5]
  • S. m. bv. mediterranense [6]
  • S. m. bv. meliloti
  • S. m. bv. rigiduloides [7]
  • S. m. ecotype NRR [8]
Synonyms [9]
  • Rhizobium meliloti Dangeard, 1926
  • Sinorhizobium meliloti (Dangeard, 1926) De Lajudie et al., 1994

Ensifer meliloti (formerly Rhizobium meliloti and Sinorhizobium meliloti) [10] are an aerobic, Gram-negative, and diazotrophic species of bacteria. S. meliloti are motile and possess a cluster of peritrichous flagella. [11] S. meliloti fix atmospheric nitrogen into ammonia for their legume hosts, such as alfalfa. S. meliloti forms a symbiotic relationship with legumes from the genera Medicago , Melilotus and Trigonella , including the model legume Medicago truncatula . This symbiosis promotes the development of a plant organ, termed a root nodule. Because soil often contains a limited amount of nitrogen for plant use, the symbiotic relationship between S. meliloti and their legume hosts has agricultural applications. [12] These techniques reduce the need for inorganic nitrogenous fertilizers. [13]

Symbiosis

Indeterminate nodule Indeterminate Nodule Zonation.JPG
Indeterminate nodule

Symbiosis between S. meliloti and its legume hosts begins when the plant secretes an array of betaines and flavonoids into the rhizosphere: 4,4′-dihydroxy-2′-methoxychalcone, [14] chrysoeriol, [15] cynaroside, [15] 4′,7-dihydroxyflavone, [14] 6′′-O-malonylononin, [16] liquiritigenin, [14] luteolin, [17] 3′,5-dimethoxyluteolin, [15] 5-methoxyluteolin, [15] medicarpin, [16] stachydrine, [18] and trigonelline. [18] These compounds attract S. meliloti to the surface of the root hairs of the plant where the bacteria begin secreting nod factors. This initiates root hair curling. The rhizobia then penetrate the root hairs and proliferate to form an infection thread. Through the infection thread, the bacteria move toward the main root. The bacteria develop into bacteroids within newly formed root nodules and perform nitrogen fixation for the plant. A S. meliloti bacterium does not perform nitrogen fixation until it differentiates into a endosymbiotic bacteroid. A bacteroid depends on the plant for survival. [19]

Leghemoglobin, produced by leguminous plants after colonization of S. meliloti, interacts with the free oxygen in the root nodule where the rhizobia reside. Rhizobia are contained within symbiosomes in the root nodules of leguminous plants. The leghemoglobin reduces the amount of free oxygen present. Oxygen disrupts the function of the nitrogenase enzyme in the rhizobia, which is responsible for nitrogen fixation. [20]

Genome

The S. meliloti genome contains four genes coding for flagellin. These include fliC1C2–fliC3C4. [11] The genome contains three replicons: a chromosome (~3.7 megabases), a chromid (pSymB; ~1.7 megabases), and a plasmid (pSymA; ~1.4 megabases). Individual strains may possess additional, accessory plasmids. Five S. meliloti genomes have been sequenced to date: Rm1021, [21] AK83, [22] BL225C, [22] Rm41, [23] and SM11 [24] with 1021 considered to be the wild type. Indeterminate nodule symbiosis by S. meliloti is conferred by genes residing on pSymA. [25]

DNA repair

The proteins encoded by E. meliloti genes uvrA, uvrB and uvrC are employed in the repair of DNA damages by the process of nucleotide excision repair. E. meliloti is a desiccation tolerant bacterium. However, E. meliloti mutants defective in either genes uvrA, uvrB or uvrC are sensitive to desiccation, as well as to UV light. [26] This finding indicates that the desiccation tolerance of wild-type E. meliloti depends on the repair of DNA damages that can be caused by desiccation.

Bacteriophage

Plaques in S. meliloti caused by PhM12. PhM12 Plaques in Sinorhizobium meliloti.JPG
Plaques in S. meliloti caused by ΦM12.

Several bacteriophages that infect Sinorhizobium meliloti have been described: [27] Φ1, [28] Φ1A, [29] Φ2A, [29] Φ3A, [30] Φ4 (=ΦNM8), [31] Φ5t (=ΦNM3), [31] Φ6 (=ΦNM4), [31] Φ7 (=ΦNM9), [31] Φ7a, [28] Φ9 (=ΦCM2), [31] Φ11 (=ΦCM9), [31] Φ12 (=ΦCM6), [31] Φ13, [32] Φ16, [32] Φ16-3, [33] Φ16a, [32] Φ16B, [30] Φ27, [28] Φ32, [33] Φ36, [33] Φ38, [33] Φ43, [28] Φ70, [28] Φ72, [33] Φ111, [33] Φ143, [33] Φ145, [33] Φ147, [33] Φ151, [33] Φ152, [33] Φ160, [33] Φ161, [33] Φ166, [33] Φ2011, [34] ΦA3, [28] ΦA8, [28] ΦA161, [34] ΦAL1, [35] ΦCM1, [34] ΦCM3, [34] ΦCM4, [34] ΦCM5, [34] ΦCM7, [34] ΦCM8, [34] ΦCM20, [34] ΦCM21, [34] ΦDF2, [35] Φf2D, [35] ΦF4, [36] ΦFAR, [35] ΦFM1, [34] ΦK1, [37] ΦL1, [32] ΦL3, [32] ΦL5, [32] ΦL7, [32] ΦL10, [32] ΦL20, [32] ΦL21, [32] ΦL29, [32] ΦL31, [32] ΦL32, [32] ΦL53, [32] ΦL54, [32] ΦL55, [32] ΦL56, [32] ΦL57, [32] ΦL60, [32] ΦL61, [32] ΦL62, [32] ΦLO0, [35] ΦLS5B, [34] ΦM1, [27] [38] ΦM1, [27] [39] ΦM1-5, [34] ΦM2, [40] ΦM3, [28] ΦM4, [28] ΦM5, [27] [28] [41] ΦM5 (=ΦF20), [27] [38] ΦM5N1, [34] ΦM6, [38] ΦM7, [38] ΦM8, [40] ΦM9, [38] ΦM10, [38] ΦM11, [38] ΦM11S, [34] ΦM12, [38] [42] ΦM14, [38] ΦM14S, [34] ΦM19, [43] ΦM20S, [34] [44] ΦM23S, [34] ΦM26S, [34] ΦM27S, [34] ΦMl, [45] ΦMM1C, [34] ΦMM1H, [34] ΦMP1, [46] ΦMP2, [46] ΦMP3, [46] ΦMP4, [46] ΦN2, [28] ΦN3, [28] ΦN4, [28] ΦN9, [28] ΦNM1, [34] [44] ΦNM2, [34] [44] ΦNM6, [34] [44] ΦNM7, [34] [44] ΦP6, [36] ΦP10, [36] ΦP33, [36] ΦP45, [36] ΦPBC5, [47] ΦRm108, [48] ΦRmp26, [49] ΦRmp36, [49] ΦRmp38, [49] ΦRmp46, [49] ΦRmp50, [49] ΦRmp52, [49] ΦRmp61, [49] ΦRmp64, [49] ΦRmp67, [49] ΦRmp79, [49] ΦRmp80, [49] ΦRmp85, [49] ΦRmp86, [49] ΦRmp88, [49] ΦRmp90, [49] ΦRmp145, [49] ΦSP, [28] ΦSSSS304, [50] ΦSSSS305, [50] ΦSSSS307, [50] ΦSSSS308, [50] and ΦT1. [28] Of these, ΦM5, [41] ΦM12, [42] Φ16-3 [51] and ΦPBC5 [47] have been sequenced.

As of March 2020 the International Committee on Taxonomy of Viruses (ICTV) has accepted the following species in its Master Species List 2019.v1 (#35):

  • Species: Sinorhizobium virus M7 (alias ΦM7) [38]
  • Species: Sinorhizobium virus M12 (alias DNA phage ΦM12, type species) [38]
  • Species: Sinorhizobium virus N3 (alias ΦN3) [28]

Related Research Articles

<span class="mw-page-title-main">Rhizobia</span> Nitrogen fixing soil bacteria

Rhizobia are diazotrophic bacteria that fix nitrogen after becoming established inside the root nodules of legumes (Fabaceae). To express genes for nitrogen fixation, rhizobia require a plant host; they cannot independently fix nitrogen. In general, they are gram negative, motile, non-sporulating rods.

<i>Rhizobium</i> Genus of nitrogen-fixing bacteria

Rhizobium is a genus of Gram-negative soil bacteria that fix nitrogen. Rhizobium species form an endosymbiotic nitrogen-fixing association with roots of (primarily) legumes and other flowering plants.

<span class="mw-page-title-main">Root nodule</span> Plant part

Root nodules are found on the roots of plants, primarily legumes, that form a symbiosis with nitrogen-fixing bacteria. Under nitrogen-limiting conditions, capable plants form a symbiotic relationship with a host-specific strain of bacteria known as rhizobia. This process has evolved multiple times within the legumes, as well as in other species found within the Rosid clade. Legume crops include beans, peas, and soybeans.

<span class="mw-page-title-main">Nod factor</span> Signaling molecule

Nod factors, are signaling molecules produced by soil bacteria known as rhizobia in response to flavonoid exudation from plants under nitrogen limited conditions. Nod factors initiate the establishment of a symbiotic relationship between legumes and rhizobia by inducing nodulation. Nod factors produce the differentiation of plant tissue in root hairs into nodules where the bacteria reside and are able to fix nitrogen from the atmosphere for the plant in exchange for photosynthates and the appropriate environment for nitrogen fixation. One of the most important features provided by the plant in this symbiosis is the production of leghemoglobin, which maintains the oxygen concentration low and prevents the inhibition of nitrogenase activity.

Sharon Rugel Long is an American plant biologist. She is the Steere-Pfizer Professor of Biological Science in the Department of Biology at Stanford University, and the Principal Investigator of the Long Laboratory at Stanford.

<i>suhB</i>

suhB, also known as mmgR, is a non-coding RNA found multiple times in the Agrobacterium tumefaciens genome and related alpha-proteobacteria. Other non-coding RNAs uncovered in the same analysis include speF, ybhL, metA, and serC.

<i>Bradyrhizobium</i> Genus of bacteria

Bradyrhizobium is a genus of Gram-negative soil bacteria, many of which fix nitrogen. Nitrogen fixation is an important part of the nitrogen cycle. Plants cannot use atmospheric nitrogen (N2); they must use nitrogen compounds such as nitrates.

<i>Ensifer</i> (bacterium) Genus of bacteria

Ensifer is a genus of nitrogen-fixing bacteria (rhizobia), three of which have been sequenced.

Bradyrhizobium japonicum is a species of legume-root nodulating, microsymbiotic nitrogen-fixing bacteria. The species is one of many Gram-negative, rod-shaped bacteria commonly referred to as rhizobia. Within that broad classification, which has three groups, taxonomy studies using DNA sequencing indicate that B. japonicum belongs within homology group II.

<span class="mw-page-title-main">ENOD40</span>

enod40, also known as early nodulin 40, is a gene found in flowering plants. The gene has characteristics of both protein and Non-coding RNA genes. There is some evidence that the non-coding characteristics of this gene are more widely conserved than the protein coding sequences. In soyabeans enod40 was found to be expressed during early stages of formation of nitrogen-fixing root nodules that are associated with symbiotic soil rhizobial bacteria. The gene is also active in roots containing fungi forming phosphate-acquiring arbuscular mycorrhiza. An interaction with a novel RNA-binding protein MtRBP1 investigated in the development of Root nodule suggests ENOD40 has a function of cytoplasmic relocalization of nuclear proteins. In the study of non-legume plants, the over-expression of ENOD40 in transgenic Arabidopsis lines was observed a reduction of cell expansion.

<span class="mw-page-title-main">Medicarpin</span> Chemical compound

Medicarpin is a pterocarpan, a derivative of isoflavonoids.

Small non-coding RNAs in the endosymbiotic diazotroph α-proteobacterium <i>Sinorhizobium meliloti</i>

Within genetics, post-genomic research has rendered bacterial small non-coding RNAs (sRNAs) as major players in post-transcriptional regulation of gene expression in response to environmental stimuli. The Alphaproteobacteria includes Gram-negative microorganisms with diverse life styles; frequently involving long-term interactions with higher eukaryotes.

αr7 is a family of bacterial small non-coding RNAs with representatives in a broad group of Alphaproteobacterial species from the order Hyphomicrobiales. The first member of this family was found in a Sinorhizobium meliloti 1021 locus located in the chromosome (C). Further homology and structure conservation analysis identified full-length homologs in several nitrogen-fixing symbiotic rhizobia, in the plant pathogens belonging to Agrobacterium species as well as in a broad spectrum of Brucella species. αr7 RNA species are 134-159 nucleotides (nt) long and share a well defined common secondary structure. αr7 transcripts can be catalogued as trans-acting sRNAs expressed from well-defined promoter regions of independent transcription units within intergenic regions (IGRs) of the Alphaproteobacterial genomes.

αr14 is a family of bacterial small non-coding RNAs with representatives in a broad group of α-proteobacteria. The first member of this family (Smr14C2) was found in a Sinorhizobium meliloti 1021 locus located in the chromosome (C). It was later renamed NfeR1 and shown to be highly expressed in salt stress and during the symbiotic interaction on legume roots. Further homology and structure conservation analysis identified 2 other chromosomal copies and 3 plasmidic ones. Moreover, full-length Smr14C homologs have been identified in several nitrogen-fixing symbiotic rhizobia, in the plant pathogens belonging to Agrobacterium species as well as in a broad spectrum of Brucella species. αr14C RNA species are 115-125 nt long and share a well defined common secondary structure. Most of the αr14 transcripts can be catalogued as trans-acting sRNAs expressed from well-defined promoter regions of independent transcription units within intergenic regions (IGRs) of the α-proteobacterial genomes.

αr15 is a family of bacterial small non-coding RNAs with representatives in a broad group of α-proteobacteria from the order Rhizobiales. The first members of this family were found tandemly arranged in the same intergenic region (IGR) of the Sinorhizobium meliloti 1021 chromosome (C). Further homology and structure conservation analysis have identified full-length Smr15C1 and Smr15C2 homologs in several nitrogen-fixing symbiotic rhizobia, in the plant pathogens belonging to Agrobacterium species as well as in a broad spectrum of Brucella species. The Smr15C1 and Smr15C2 homologs are also encoded in tandem within the same IGR region of Rhizobium and Agrobacterium species, whereas in Brucella species the αr15C loci are spread in the IGRs of Chromosome I. Moreover, this analysis also identified a third αr15 loci in extrachromosomal replicons of the mentioned nitrogen-fixing α-proteobacteria and in the Chromosome II of Brucella species. αr15 RNA species are 99-121 nt long and share a well defined common secondary structure consisting of three stem loops. The transcripts of the αr15 family can be catalogued as trans-acting sRNAs encoded by independent transcription units with recognizable promoter and transcription termination signatures within intergenic regions (IGRs) of the α-proteobacterial genomes.

αr45 is a family of bacterial small non-coding RNAs with representatives in a broad group of α-proteobacteria from the order Hyphomicrobiales. The first member of this family (Smr45C) was found in a Sinorhizobium meliloti 1021 locus located in the chromosome (C). Further homology and structure conservation analysis identified homologs in several nitrogen-fixing symbiotic rhizobia, in the plant pathogens belonging to Agrobacterium species as well as in a broad spectrum of Brucella species, in Bartonella species, in several members of the Xanthobactereacea family, and in some representatives of the Beijerinckiaceae family. αr45C RNA species are 147-153 nt long and share a well defined common secondary structure. All of the αr45 transcripts can be catalogued as trans-acting sRNAs expressed from well-defined promoter regions of independent transcription units within intergenic regions (IGRs) of the α-proteobacterial genomes.

Ensifer fredii is a nitrogen fixing bacterium. It is a fast-growing root nodule bacterium. Ensifer fredii exhibits a broad host-range and is able to nodulate both determinant hosts, such as soy, as well as indeterminate hosts including the pigeon pea. Because of their ease of host infection there is interest in their genetics and the symbiotic role in host infection and nodule formation.

Mesorhizobium mediterraneum is a bacterium from the genus Mesorhizobium, which was isolated from root nodule of the Chickpea in Spain. The species Rhizobium mediterraneum was subsequently transferred to Mesorhizobium mediterraneum. This species, along with many other closely related taxa, have been found to promote production of chickpea and other crops worldwide by forming symbiotic relationships.

Ensifer medicae is a species of gram-negative, nitrogen-fixing, rod-shaped bacteria. They can be free-living or symbionts of leguminous plants in root nodules. E.medicae was first isolated from root nodules on plants in the genus Medicago. Some strains of E.medicae, like WSM419, are aerobic. They are chemoorganotrophic mesophiles that prefer temperatures around 28 °C. In addition to their primary genome, these organisms also have three known plasmids, sized 1,570,951 bp, 1,245,408 bp and 219,313 bp.

<span class="mw-page-title-main">Symbiosome</span>

A symbiosome is a specialised compartment in a host cell that houses an endosymbiont in a symbiotic relationship.

References

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  23. ↑ The sequence hasn't been officially announced, but is available at NCBI: chromosome, pSymA, pSymB, and pRM41a.
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  27. 1 2 3 4 5 Systematic naming of bacteriophages is rarely followed in the scientific literature, and a variety of phages can share the same name. While there exists an RNA phage called ΦM12, which infects enterobacteria, it is not synonymous with the DNA phage ΦM12 listed here. The same may be true for other phages in this list. Within this list, two phages have independently been named ΦM5.
  28. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Lesley SM (1982). "A bacteriophage typing system for Rhizobium meliloti". Canadian Journal of Microbiology. 28 (2): 180–189. doi:10.1139/m82-024.
  29. 1 2 Singh RB, Dhar B, Singh BD (1986). "Morphology and general characteristics of viruses active against cowpea Rhizobium CB756 and 32H1". Archives of Virology. 64 (1): 17–24. doi:10.1002/jobm.3620270309. PMID   7377972. S2CID   84732610.
  30. 1 2 Handelsman J, Ugalde RA, Brill WJ (March 1984). "Rhizobium meliloti competitiveness and the alfalfa agglutinin". Journal of Bacteriology. 157 (3): 703–7. doi:10.1128/JB.157.3.703-707.1984. PMC   215314 . PMID   6698937.
  31. 1 2 3 4 5 6 7 Krsmanovi-Simic D, Werquin M (1977). "Etude des bactériophages de Rhizobium meliloti" [Study of bacteriophages of Rhizobium meliloti]. Comptes Rendus de l'Académie des Sciences, Série D (in French). 284: 1851–1854. and Krsmanovi-Simic D, Werquin M (1973). "Etude des bactériophages de Rhizobium meliloti" [Study of bacteriophages of Rhizobium meliloti]. Comptes Rendus de l'Académie des Sciences, Série D (in French). 276 (19): 2745–8. PMID   4198859.
  32. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 Kowalski M (1967). "Transduction in Rhizobium meliloti". Acta Microbiologica Polonica. 16 (1): 7–11. doi:10.1007/BF02661838. PMID   4166074. S2CID   10908418. Note that this article was reprinted in Plant and Soil (1971) 35 (1): 63—66, which is where the URL and doi direct to.
  33. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 Szende K, Ördögh F (1960). "Die Lysogenie von Rhizobium meliloti". Naturwissenschaften. 47 (17): 404–405. Bibcode:1960NW.....47..404S. doi:10.1007/BF00631269. S2CID   44438409.
    The full genome of this phage is available at NCBI
  34. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Werquin M, Ackermann HW, Levesque RC (January 1988). "A Study of 33 Bacteriophages of Rhizobium meliloti". Applied and Environmental Microbiology. 54 (1): 188–196. doi:10.1128/AEM.54.1.188-196.1988. PMC   202420 . PMID   16347525.
  35. 1 2 3 4 5 Corral E, Montoya E, Olivares J (1978). "Sensitivity to phages in Rhizobium meliloti as a plasmid consequence". Microbios Letters. 5: 77–80.
  36. 1 2 3 4 5 Kowalski M, Małek W, Czopska-Dolecka J, Szlachetka M (2004). "The effect of rhizobiophages on Sinorhizobium meliloti–Medicago sativa symbiosis". Biology and Fertility of Soils. 39 (4): 292–294. doi:10.1007/s00374-004-0721-y. S2CID   26352194.
  37. ↑ Wdowiak S, Małek W, Grzadka M (February 2000). "Morphology and general characteristics of phages specific for Astragalus cicer rhizobia". Current Microbiology. 40 (2): 110–3. doi:10.1007/s002849910021. PMID   10594224. S2CID   5181655.
  38. 1 2 3 4 5 6 7 8 9 10 11 Finan TM, Hartweig E, LeMieux K, Bergman K, Walker GC, Signer ER (July 1984). "General transduction in Rhizobium meliloti". Journal of Bacteriology. 159 (1): 120–4. doi:10.1128/JB.159.1.120-124.1984. PMC   215601 . PMID   6330024.
  39. ↑ Małek W (1990). "Properties of the transducing phage M1 of Rhizobium meliloti". Journal of Basic Microbiology. 30 (1): 43–50. doi:10.1002/jobm.3620300114. S2CID   86226063.
  40. 1 2 Johansen E, Finan TM, Gefter ML, Signer ER (October 1984). "Monoclonal antibodies to Rhizobium meliloti and surface mutants insensitive to them". Journal of Bacteriology. 160 (1): 454–7. doi:10.1128/JB.160.1.454-457.1984. PMC   214744 . PMID   6480561.
  41. 1 2 Johnson MC, Sena-Veleza M, Washburn BK, Platta GN, Lua S, Brewer TE, Lynna JS, Stroupe ME, Jones KM (December 2017). "Structure, proteome and genome of Sinorhizobium meliloti phage ΦM5: A virus with LUZ24-like morphology and a highly mosaic genome". Journal of Structural Biology. 200 (3): 343–359. doi: 10.1016/j.jsb.2017.08.005 . PMID   28842338.
  42. 1 2 Brewer Tess E, Elizabeth Stroupe M, Jones Kathryn M (Dec 25, 2013). "The genome, proteome and phylogenetic analysis of Sinorhizobium meliloti phage ΦM12, the founder of a new group of T4-superfamily phages". Virology. 450–451: 84–97. doi: 10.1016/j.virol.2013.11.027 . PMID   24503070.
  43. ↑ Campbell GR, Reuhs BL, Walker GC (October 1998). "Different phenotypic classes of Sinorhizobium meliloti mutants defective in synthesis of K antigen". Journal of Bacteriology. 180 (20): 5432–6. doi:10.1128/JB.180.20.5432-5436.1998. PMC   107593 . PMID   9765576.
  44. 1 2 3 4 5 Werquin M, Ackermann HW, Levesque RC (1989). "Characteristics and comparative study of five Rhizobium meliloti bacteriophages". Current Microbiol. 18 (5): 307–311. doi:10.1007/BF01575946. S2CID   11937563.
  45. ↑ Małek W (1990). "Properties of the transducing phage Ml of Rhizobium meliloti". Journal of Basic Microbiology. 30 (1): 43–50. doi:10.1002/jobm.3620300114. S2CID   86226063. Archived from the original on 2013-01-05.
  46. 1 2 3 4 Martin MO, Long SR (July 1984). "Generalized transduction in Rhizobium meliloti". Journal of Bacteriology. 159 (1): 125–9. doi:10.1128/JB.159.1.125-129.1984. PMC   215602 . PMID   6330025.
  47. 1 2 This phage has never been formally reported in the scientific literature. However, the full genomic sequence has been uploaded to NCBI, available here.
  48. ↑ Novikova NI, Bazenova OV, Simarov BV (1987). "Phage sensitivity of natural and mutant strains of alfalfa nodule bacteria differing by cultural and symbiotic properties. (Summary in English)". Agric. Biol. 2: 35–39.
  49. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Khanuja SP, Kumar S (1989). "Symbiotic and galactose utilization properties of phage RMP64-resistant mutants affecting three complementation groups in Rhizobium meliloti". Journal of Genetics. 68 (2): 93–108. doi:10.1007/BF02927852. S2CID   25258531.
  50. 1 2 3 4 Sharma RS, Mishra V, Mohmmed A, Babu CR (April 2008). "Phage specificity and lipopolysaccarides of stem- and root-nodulating bacteria (Azorhizobium caulinodans, Sinorhizobium spp., and Rhizobium spp.) of Sesbania spp". Archives of Microbiology. 189 (4): 411–8. doi:10.1007/s00203-007-0322-x. PMID   17989956. S2CID   5746480.
  51. ↑ Φ16-3 Complete Genome

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