Rhizobial Symbiovars

Some members of the Sc published a paper “Guidelines for the description ofrhizobial symbiovars”. In this paper, they discussed the requirements and guidelines to describe symbiovars, propose a set of rules, provide a list of all symbiovars published so far, and offer a mechanism to maintain a list in the future.

Proposed guidelines for the description and naming of symbiovars

1. Description

1a. Plant specificity is the essential basis to define a symbiovar. Symbiovars should be described in relation to the symbiosis phenotypes, not only referring to nodulation but also to effectiveness by considering nitrogen fixation.

1b. A symbiovar must have a representative strain, and the genome sequence of that strain must be publicly available and of sufficient quality. It is recommended (but not obligatory) that the representative strain be available in an international culture collection.

1c. It must be demonstrated that the symbiosis genes are recognizably distinct from those of all previously described symbiovars in sequence or in the presence/absence of specific genes.

2. Naming

2a. The name of a new symbiovar must be distinct from all previously recognised symbiovar names in all genera.

2b. Symbiovar names that are adjectival always take the feminine gender.

2c. In other respects, the names of symbiovars follow the same rules as those of species epithets.

2d. A proposal for a new symbiovar must be published in the body (not supplementary files) of an article in a peer-reviewed journal, and must include all the information required by these guidelines.

3. Recognition

3a. The ICSP Subcommittee for Rhizobia and Agrobacteria undertakes to maintain a list of recognized symbiovars and to appoint persons to manage this.

3b. After publication, authors should submit the publication to the Secretary of the ICSP Subcommittee for Rhizobia and Agrobacteria.

3c. New symbiovars that conform to the guidelines and have priority will be added to the online list of recognized symbiovars on the Subcommittee website (currently https://sites.google.com/view/taxonomyagrorhizo/home).

3d. The priority of names is established by the date of inclusion in the list.

Conclusion

In view of the large number of symbiovars described so far, and the likelihood that the number will increase in the future when more legumes are thoroughly studied, we felt the need to consider some appropriate standards and to clarify the status of the symbiovars already described.  We have proposed guidelines for the description and naming of symbiovars and offered to set up and maintain a public list as a service to the rhizobial research community. Our aim is to make it easier to understand and use the symbiovar concept. As with any new venture, we may find we need to make adjustments in the light of experience, and we welcome feedback from users.

A list of all symbiovars (in alphabetical order) proposed to date is given in Table 1 in the published paper. 

 

As we discussed in the 2022 annual meeting of the subcommittee (Minute13; Mousavi and Young, Int J Syst Evol Microbiol 2023; doi:10.1099/ijsem.0.005856), Esperanza Martinez-Romero and Alvaro Peix provided the list of symbiovars of the genera Bradyrhizobium, Ensifer, Mesorhizobium, and Rhizobium.

 

Minute 13. The list of rhizobial symbiovars

 

In the case of rhizobia, we use the term symbiotic variant (symbiovar), which is a parallel term to pathovar in pathogenic bacteria [11]. Symbiovars are host-specific types that are conveyed by sets of genes usually on plasmids or mobile elements. Even though they determine many interesting properties, there is no official body regulating the names and we lack a central record for researchers to find the existing symbiovars of rhizobia. It was agreed that our Subcommittee would take on responsibility for the nomenclature of symbiovars. The first task is to provide a list of described symbiovars and the relevant publications. Esperanza Martinez-Romero took the responsibility of preparing the list of symbiovars with a small group of Subcommittee members, and the list will be uploaded in our Subcommittee blog.

Currently, there is no precise guideline for defining new symbiovars. Therefore, our Subcommittee members suggested that we should propose some minimal standards to determine rhizobial symbiovars, including levels of sequence similarity and data on host specificity.

 List of symbiovars of Rhizobium species

Symbiovar	Rhizobium species	Host	Reference
gallicum	R. azibense R. gallicum	Phaseolus vulgaris Mimosa Sesbania and others	Mnsari et al. (2014) Amarger et al. (1997)
mimosae	R. etli R. phaseoli R.sophoriradicis	Mimosa	Wang et al 1999  Rogel et al 2011 2014
phaseoli	R. anhuiense R. acidisoli R. chutanense R. ecuadorense R. etli R. esperanzae R. hidalgonense R. leguminosarum R. lusitanum R. phaseoli R. vallis	Phaseolus vulgaris	Amarger et al. (1997) Mousavi et al. (2015) Román-Ponce et al. (2016) Huo et al. (2019) Ribeiro et al. (2015) Segovia et al. (1993) Cordeiro et al. (2017) Yan et al. (2017) Valverde et al. (2006) Ormeño-Orrillo et al. (2012) Dangeard (1926) Ramírez-Bahena et al. (2008) Wang et al. (2011) Zhang et al (2015)
trifolii	R.anhuiense R.hidalgonense/acidisoli R.laguerreae R. bengladeshense R. aegypticum R. aethiopicum R.pisi	clover Trifolium alexandrinum Phaseolus vulgaris	Zhang et al 2015 Shamseldin et la 2016 Youseif et al 2021 Martínez-Hidalgo 2015 Jordan 1984
tropici	R. tropici Rhizobium freirei Rhizobium leucaenae Rhizobium lusitanum Rhizobium sp. (from Phaseolus dumosus)	Leucaena Phaseolus and others	Ormeño-Orrillo et al. (2012) Dall’Agnol et al. (2013) Ribeiro et al. (2012) Valverde et al. (2006) Martínez-Romero et al. (1991) Ramírez-Puebla et al 2019
viciae	R.anhuiense R. leguminosarum R.laguerreae R.pisi R.fabae R.multihospitium R. acidosoli	pea lentils Vicia faba Phaseolus vulgaris	Zhang et al 2015 Martinez-Hidalgo et al 2015 Jordan 1984 Boivin et al 2021 El Idrissi et al 2020 Flores-Felix 2019

 

 

List of symbiovars of Bradyrhizobium species

 

Symbiovar	Bradyrhizobium species	Host	Reference
	japonicum group
cajani	B. cajani and  other nine species	Cajanus Arachis Chamaecrista ErythrinaGlycine Inga Vigna	Klepa et al 2022
centrosemae	B. centrosemae	Centrosema	Ramírez-Bahena et al 2016
cyanophyllae	Bradyrhizobium spp.	Acacia saligna	Hsouna et al 2022
genistearum	B. canariense B.hipponense	Genista Leucaena leucocephala	Vinuesa et al 2005 Ramírez-Bahena et al 2020 Reijili et al 2020
glycinarum	B.japonicum B. daqingense B.nanningense	Glycine soja Arachis hypogaea	Vinuesa et al 2005 Klepa et al 2022  Li et al 2019
phaseolarum	B. americanum	Centrosema	Ramírez-Bahena et al 2016
sierranevadense	Bradyrhizobium sp.	Genista versicolor	Cobo-Diaz et al 2014
vignae	Bradyrhizobium group II	Vigna unguiculata	Bejarano et al 2014
	elkanii group
cenepequi	B. cenepequi	Vigna unguiculata	Klepa et al 2022
glycinis	B. australafricanum	Glycine sp.	Klepa et al 2022
lupini	B. valentinum B. retamae	Lupinus micranthus	Msaddak et al 2018
pachyrhizi	B. pachyrhizi	Arachis hypogaea	Delamuta et al 2017
retamae	B. lablabi B. retamae other species	Lablab Retama	Guerrouj et al 2013 Klepa et al 2022
septentrionali	B. septentrionale B. quebecense	native Canadian legumes and soybean	Bromfield & Cloutier 2021
soja	B.brasilense	soybean	Delamuta et al 2017
tropici	B. viridifuturi	Centrosema	Ramírez-Bahena et al 2016

 

 

 

 

List of symbiovars of Mesorhizobium species

Symbiovar	Mesohizobium species	Host	Reference
loti	M. loti M. japonicum M. helmanticense M. tamadayense M. erdmanii M. olivaresii M. sanjuani	Lotus berthelotii Lotus corniculatus Lotus japonicum Lotus tenuis Lotus lancerottensis	Ramírez-Bahena et al., 2012 Martínez-Hidalgo et al., 2016 Lorite et al., 2016 Marcos García et al., 2017 Sannazzaro et al., 2018 Duan et al., 2022
canariense	M. neociceri	Cicer canariense	León-Barrios et al., 2021
caraganae	M. caraganae	Cicer canariense	León-Barrios et al., 2021
anthyllidis	M. delmonti M. prunaderense M. metallidurans M. ventifaucium M. escarrei	Anthyllis vulneraria	Mohamad et al., 2017 Mohamad et al., 2022
sophorae	M. sophorae M. waimense	Sophora microphylla Sophora longicarinata	De Meyer et al., 2015, 2016
ciceri	M. ciceri M. wenxiniae M. amorphae	Cicer arietinum	Rivas et al., 2007  Zhang et al., 2018
glycyphyllae	Mesorhizobium sp.	Astragalus glycyphyllos	Gnat et al., 2015
albiziae	M. albiziae	Albizia kalkora	Wang et al., 2007 Duan et al., 2022
biserrulae	M. ciceri M. australicum M. opportunistum	Biserrula pelecinus	Nandasena et al., 2007
astragali	M. qingshengii M. huakuii M. jarvisii	Astragalus sinicus	Zhang et al., 2018
sesbaniae	M. hawassense	Sesbania sesban	Duan et al., 2022
psoraleae	M. chacoense	Bituminaria bituminosa	Rejili et al., 2020
aridi	M. camelthorni	Sulla spinosissima	Lamin et al., 2021
oxytropis	Mesorhizobium sp. M. loti M. huakuii	Oxytropis nigrescens	Duan et al., 2022
maamori	Mesorhizobium sp.	Ononis repens	Laadraoui et al 2022

 

 

 

List of symbiovars of Ensifer species

Symbiovar	Ensifer species	Host	Reference
acaciae	E. terangae E sahelense E. meliloti	Acacia sp. Acacia tortilis	Lortet et al., 1996 Haukka et al., 1998 Ba et al., 2022
acaciellae	E. chiapanecum E. mexicanum	Acaciella angustissima	Rogel et al., 2011
meliloti	E. meliloti E. medicae	Medicago sativa Medicago truncatula Trigonella phoenum-graecum Lotus creticus lotus pusillus	Villegas et al., 2006 Ramírez-Bahena et al., 2015 Rejili et al., 2020
medicaginis	E. meliloti	Medicago laciniata	Villegas et al., 2006
mediterranense	S. americanum	Phaseolus vulgaris	Mnasri et al 2007, 2012
rigiduloides	E. meliloti	Medicago rigiduloides	Gubry-Rangin et al., 2013
aegeanense	E. fredii	Vigna unguiculata	Tampakaki er al., 2017
sesbaniae	E. saheli E. terangae	Sesbania sp. Sesbania cannabina	Lortet et al., 1996  Zhang et al., 2020
lancerottense	E. meliloti	Lotus creticus Lotus lancerottensis	León-Barrios et al., 2009, 2017 Belechheb et al., 2021
vachelliae	E. fredii	Vachellia gummifera	Bouhnik et al., 2019
fredii	E. fredii	Glycine max	Mnasri et al 2007