Host-Associated Rhizobial Fitness: Dependence on Nitrogen, Density, Community Complexity, and Legume Genotype

Liana T. Burghardt, Brendan Epstein, Michelle Hoge, Diana I. Trujillo, Peter Tiffin

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

The environmental context of the nitrogen-fixing mutualism between leguminous plants and rhizobial bacteria varies over space and time. Variation in resource availability, population density, and composition likely affect the ecology and evolution of rhizobia and their symbiotic interactions with hosts. We examined how host genotype, nitrogen addition, rhizobial density, and community complexity affected selection on 68 rhizobial strains in the Sinorhizobium meliloti-Medicago truncatula mutualism. As expected, host genotype had a substantial effect on the size, number, and strain composition of root nodules (the symbiotic organ). The understudied environmental variable of rhizobial density had a stronger effect on nodule strain frequency than the addition of low nitrogen levels. Higher inoculum density resulted in a nodule community that was less diverse and more beneficial but only in the context of the more selective host genotype. Higher density resulted in more diverse and less beneficial nodule communities with the less selective host. Density effects on strain composition deserve additional scrutiny as they can create feedback between ecological and evolutionary processes. Finally, we found that relative strain rankings were stable across increasing community complexity (2, 3, 8, or 68 strains). This unexpected result suggests that higher-order interactions between strains are rare in the context of nodule formation and development. Our work highlights the importance of examining mechanisms of density-dependent strain fitness and developing theoretical predictions that incorporate density dependence. Furthermore, our results have translational relevance for overcoming establishment barriers in bioinoculants and motivating breeding programs that maintain beneficial plant-microbe interactions across diverse agroecological contexts. IMPORTANCE Legume crops establish beneficial associations with rhizobial bacteria that perform biological nitrogen fixation, providing nitrogen to plants without the economic and greenhouse gas emission costs of chemical nitrogen inputs. Here, we examine the influence of three environmental factors that vary in agricultural fields on strain relative fitness in nodules. In addition to manipulating nitrogen, we also use two biotic variables that have rarely been examined: the rhizobial community's density and complexity. Taken together, our results suggest that (i) breeding legume varieties that select beneficial strains despite environmental variation is possible, (ii) changes in rhizobial population densities that occur routinely in agricultural fields could drive evolutionary changes in rhizobial populations, and (iii) the lack of higherorder interactions between strains will allow the high-throughput assessments of rhizobia winners and losers during plant interactions.

Original languageEnglish (US)
JournalApplied and environmental microbiology
Volume88
Issue number15
DOIs
StatePublished - Aug 2022

Bibliographical note

Funding Information:
This work was supported by the National Science Foundation (NSF) awards IOS-1724993 and IOS-1856744 (to L.T.B. and P.T.). Any opinions, findings, conclusions, or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the NSF. L.T.B.’s work was additionally supported by the USDA National Institute of Food and Agriculture Federal Appropriations under PEN04760 and accession no. 1025611.

Publisher Copyright:
Copyright © 2022 Burghardt et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

Keywords

  • Medicago truncatula
  • Sinorhizobium (Ensifer) meliloti
  • community complexity
  • genotype x environment interaction
  • host-microbe interaction
  • inoculation density
  • legume-rhizobia
  • nitrogen addition
  • nodules
  • strain relative fitness

PubMed: MeSH publication types

  • Journal Article
  • Research Support, U.S. Gov't, Non-P.H.S.

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