1887

Microbiology Society logo

Volume 167, Issue 4

The impact of intra-specific diversity in the rhizobia-legume symbiosis Open Access

Abstract

Rhizobia - nitrogen-fixing, root-nodulating bacteria - play a critical role in both plant ecosystems and sustainable agriculture. Rhizobia form intracellular infections within legumes roots where they produce plant accessible nitrogen from atmospheric nitrogen and thus reduce the reliance on industrial inputs. The rhizobia-legume symbiosis is often treated as a pairwise relationship between single genotypes, both in research and in the production of rhizobial inoculants. However in nature individual plants are infected by a high diversity of rhizobia symbionts. How this diversity affects productivity within the symbiosis is unclear. Here, we use a powerful statistical approach to assess the impact of diversity within the clover symbiosis using a biodiversity-ecosystem function framework. Statistically, we found no significant impact of rhizobium diversity. However this relationship was weakly positive - rather than negative - indicating that there is no significant cost to increasing inoculant diversity. Productivity was influenced by the identity of the strains within an inoculant; strains with the highest individual performance showed a significant positive contribution within mixed inoculants. Overall, inoculant effectiveness was best predicted by the individual performance of the best inoculant member, and only weakly predicted by the worst performing member. Collectively, our data suggest that the clover symbiosis displays a weak diversity-function relationship, but that inoculant performance can be improved through the inclusion of high performing strains. Given the wide environmental dependence of rhizobial inoculant quality, multi-strain inoculants could be highly successful as they increase the likelihood of including a strain well adapted to local conditions across different environments.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): intraspecific diversity , multistrain inoculant , mutualism , Rhizobia , Rhizobium leguminosarum and Symbiosis
Funding
This study was supported by the:
  • Natural Environment Research Council (Award NE/P017584/1)
    • Principle Award Recipient: EllieHarrison
  • British Ecological Society (Award SR16/1349)
    • Principle Award Recipient: EllieHarrison
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001051
2021-04-08
2024-05-10
Loading full text...

Full text loading...

/deliver/fulltext/micro/167/4/mic001051.html?itemId=/content/journal/micro/10.1099/mic.0.001051&mimeType=html&fmt=ahah

References

  1. Graham PH, Vance CP. Legumes: importance and constraints to greater use. Plant Physiol 2003; 131:872–877 [View Article][PubMed]
     [Google Scholar]
  2. Deaker R, Roughley RJ, Kennedy IR. Legume seed inoculation technology?a review. Soil Biology and Biochemistry 2004; 36:1275–1288 [View Article]
     [Google Scholar]
  3. Santos MS, Nogueira MA, Hungria M. Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express 2019; 9:205 [View Article][PubMed]
     [Google Scholar]
  4. Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G et al. High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus Irregularis”. New Phytol 2018; 220:1161–1171 [View Article][PubMed]
     [Google Scholar]
  5. Kumar N, Lad G, Giuntini E, Kaye ME, Udomwong P et al. Bacterial genospecies that are not ecologically coherent: population genomics of Rhizobium Leguminosarum”. Open Biol 2015; 5:140133 [View Article][PubMed]
     [Google Scholar]
  6. Checcucci A, Azzarello E, Bazzicalupo M, Galardini M, Lagomarsino A et al. “Mixed nodule infection in Sinorhizobium meliloti–Medicago sativa symbiosis suggest the presence of cheating behavior”. Frontiers in Plant Science 7 2016; 5396:
     [Google Scholar]
  7. Siler E, Friesen ML. “Widespread negative Frequency-Dependent selection maintains diversity in the Legume-Rhizobia Symbiosis: balancing nodulation may explain the paradox of rhizobium diversity”. Cold Spring Harbor Laboratory 2017
     [Google Scholar]
  8. Parkinson JE, Banaszak AT, Altman NS, LaJeunesse TC, Baums IB. Intraspecific diversity among partners drives functional variation in coral symbioses. Sci Rep 2015; 5: [View Article]
     [Google Scholar]
  9. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 1998; 396:69–72 [View Article]
     [Google Scholar]
  10. Vogelsang KM, Reynolds HL, Bever JD. Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 2006; 172:554–562 [View Article][PubMed]
     [Google Scholar]
  11. Barrett LG, Bever JD, Bissett A, Thrall PH. Partner diversity and identity impacts on plant productivity in Acacia -rhizobial interactions. J Ecology 2015; 103:130–142 [View Article]
     [Google Scholar]
  12. Bever JD, Broadhurst LM, Thrall PH. Microbial phylotype composition and diversity predicts plant productivity and plant-soil feedbacks. Ecol Lett 2013; 16:167–174 [View Article][PubMed]
     [Google Scholar]
  13. Heath KD, Tiffin P. Context dependence in the coevolution of plant and rhizobial mutualists. Proc R Soc B 2007; 274:1905–1912 [View Article]
     [Google Scholar]
  14. Kyei-Boahen S, Nleya T, Hynes R, Walley FL. Single and Multistrain rhizobial inocula for pinto and black bean cultivars. J Plant Nutr 2005; 28:1679–1692 [View Article]
     [Google Scholar]
  15. Somasegaran P, Bohlool BB. Single-Strain versus Multistrain inoculation: effect of soil mineral N availability on rhizobial strain effectiveness and competition for nodulation on chick-pea, soybean, and dry bean. Appl Environ Microbiol 1990; 56:3298–3303 [View Article][PubMed]
     [Google Scholar]
  16. Loreau M, Hector A. Partitioning selection and complementarity in biodiversity experiments. Nature 2001; 412:72–76 [View Article][PubMed]
     [Google Scholar]
  17. Barrett LG, Bever JD. Effect of genotypes-Rhizobium-environment interaction on nodulation and productivity of common bean (Phaseolus vulgaris L.) in eastern Ethiopia. Environ Syst Res 2018; 6:14 [View Article]
     [Google Scholar]
  18. Burghardt LT. “Evolving together, evolving Apart: measuring the fitness of rhizobial bacteria in and out of symbiosis with leguminous plants”. The New Phytologist, July 2019
     [Google Scholar]
  19. Bell T, Lilley AK, Hector A, Schmid B, King L et al. A linear model method for biodiversity-ecosystem functioning experiments. Am Nat 2009; 174:836–849 [View Article][PubMed]
     [Google Scholar]
  20. Young J, Moeskjær S, Afonin A, Rahi P, Maluk M et al. Defining the Rhizobium Leguminosarum species complex. Genes 2021; 12:111 [View Article][PubMed]
     [Google Scholar]
  21. Cavassim MIA, Moeskjær S, Moslemi C, Bachmann A et al. Symbiosis genes show a unique pattern of introgression and selection within a Rhizobium leguminosarum species complex. Microbial Genomics 2020; 6: [View Article]
     [Google Scholar]
  22. Howieson JG, Dilworth MJ. Eds. n.d. working with rhizobia.
  23. Catroux G, Hartmann A, Revellin C. “Trends in rhizobial inoculant production and use”. Plant Soil 2001; 230:21–30 [View Article]
     [Google Scholar]
  24. Piha MI, Munns DN. Nitrogen fixation potential of beans (Phaseolus vulgaris L.) compared with other grain legumes under controlled conditions. Plant Soil 1987; 98:169–182 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001051
Loading
The impact of intra-specific diversity in the rhizobia-legume symbiosis
Microbiology 167, 001051 (2021); https://doi.org/10.1099/mic.0.001051
/content/journal/micro/10.1099/mic.0.001051
/content/journal/micro/10.1099/mic.0.001051
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error