Microbial symbionts exhibit broad genotypic variation in their fitness effects on hosts, leaving hosts vulnerable to costly partnerships. Interspecific conflict and partner‐maladaptation are frameworks to explain this variation, with different implications for mutualism stability. We investigated the mutualist service of nitrogen fixation in a metapopulation of root‐nodule forming
The isolation of
- PAR ID:
- 10514366
- Editor(s):
- Semrau, Jeremy D
- Publisher / Repository:
- American Society for Microbiology
- Date Published:
- Journal Name:
- Applied and Environmental Microbiology
- Volume:
- 88
- Issue:
- 22
- ISSN:
- 0099-2240
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Bradyrhizobium symbionts inAcmispon hosts. We uncoveredBradyrhizobium genotypes that provide negligible mutualist services to hosts and had superiorin planta fitness during clonal infections, consistent with cheater strains that destabilise mutualisms. Interspecific conflict was also confirmed at the metapopulation level – by a significant negative association between the fitness benefits provided byBradyrhizobium genotypes and their local genotype frequencies – indicating that selection favours cheating rhizobia. Legumes have mechanisms to defend against rhizobia that fail to fix sufficient nitrogen, but these data support predictions that rhizobia can subvert plant defenses and evolve to exploit hosts. -
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Abstract Plant hosts can gain significant growth benefits from symbiosis with microbes, but these benefits could be threatened by divergent fitness interests among partners. Here, we measured fitness outcomes in symbiosis, by varying the genotypes of both microbes and hosts, to examine scenarios that might favour uncooperative symbionts. We studied associations between Acmispon strigosus, an annual legume native to California, and its nitrogen-fixing symbionts in the genus Bradyrhizobium. Bradyrhizobium symbionts form root nodules on compatible hosts, with strains varying from effective, fixing substantial nitrogen for the host, to ineffective strains that do not fix nitrogen and provide no benefit to host growth. We co-inoculated four A. strigosus plant lines with nine combinations of effective and ineffective Bradyrhizobium strains and measured the relative fitness of ineffective strains within individual nodules, as hosts must select against uncooperative symbionts to maintain benefits. In mixed infections, ineffective strains always had lower relative fitness in nodules compared to beneficial strains, consistent with efficient punishment of non-fixing rhizobia. However, ineffective strains exhibited genotypic variation in their fitness in nodules within individual nodules co-infected with a beneficial strain, suggesting a role for symbiont competitiveness in shaping this joint phenotype. Variation in symbiont fitness during co-inoculations did not measurably affect plant performance, suggesting that predicted conflict over the joint phenotype of rhizobia fitness has negligible effect on the host.
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Buchan, Alison (Ed.)ABSTRACT The ability of Bradyrhizobium spp. to nodulate and fix atmospheric nitrogen in soybean root nodules is critical to meeting humanity’s nutritional needs. The intricacies of soybean bradyrhizobia-plant interactions have been studied extensively; however, bradyrhizobial ecology as influenced by phages has received somewhat less attention, even though these interactions may significantly impact soybean yield. In batch culture, four soybean bradyrhizobia strains, Bradyrhizobium japonicum S06B (S06B-Bj), B. japonicum S10J (S10J-Bj), Bradyrhizobium diazoefficiens USDA 122 (USDA 122-Bd), and Bradyrhizobium elkanii USDA 76 T (USDA 76-Be), spontaneously (without apparent exogenous chemical or physical induction) produced tailed phages throughout the growth cycle; for three strains, phage concentrations exceeded cell numbers by ~3-fold after 48 h of incubation. Phage terminase large-subunit protein phylogeny revealed possible differences in phage packaging and replication mechanisms. Bioinformatic analyses predicted multiple prophage regions within each soybean bradyrhizobia genome, preventing accurate identification of spontaneously produced prophage (SPP) genomes. A DNA sequencing and mapping approach accurately delineated the boundaries of four SPP genomes within three of the soybean bradyrhizobia chromosomes and suggested that the SPPs were capable of transduction. In addition to the phages, S06B-Bj and USDA 76-Be contained three to four times more insertion sequences (IS) and large, conjugable, broad host range plasmids, both of which are known drivers of horizontal gene transfer (HGT) in soybean bradyrhizobia. These factors indicate that SPP along with IS and plasmids participate in HGT, drive bradyrhizobia evolution, and play an outsized role in bradyrhizobia ecology. IMPORTANCE Previous studies have shown that IS and plasmids mediate HGT of symbiotic nodulation ( nod ) genes in soybean bradyrhizobia; however, these events require close cell-to-cell contact, which could be limited in soil environments. Bacteriophage-assisted gene transduction through spontaneously produced prophages provides a stable means of HGT not limited by the constraints of proximal cell-to-cell contact. These phage-mediated HGT events may shape soybean bradyrhizobia population ecology, with concomitant impacts on soybean agriculture.more » « less
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Abstract New genetic engineering techniques have advanced the field of plant molecular biology, and
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Abstract Legume crops such as soybean obtain a large portion of their nitrogen nutrition through symbiotic nitrogen fixation by diazotrophic rhizobia bacteria in root nodules. However, nodule occupancy by low‐capacity nitrogen‐fixing rhizobia can lead to lower‐than‐optimal levels of nitrogen fixation. Seed/root coating with engineered materials such as graphene‐carrying biomolecules that may promote specific attraction/attachment of desirable bacterial strains is a potential strategy that can help overcome this rhizobia competition problem. As a first step towards this goal, we assessed the impact of graphene on soybean and
Bradyrhizobium using a set of growth, biochemical, and physiological assays. Three different concentrations of graphene were tested for toxicity in soybean (50, 250, and 1,000 mg/l) andBradyrhizobia (25, 50, and 100 mg/l). Higher graphene concentrations (250 mg/l and 1,000 mg/l) promoted seed germination but slightly delayed plant development. Spectrometric and microscopy assays for hydrogen peroxide and superoxide anion suggested that specific concentrations of graphene led to higher levels of reactive oxygen species in the roots. In agreement, these roots also showed higher activities of antioxidant enzymes, catalase, and ascorbate peroxidase. Conversely, no toxic effects were detected onBradyrhizobia treated with graphene, and neither did they have higher levels of reactive oxygen species. Graphene treatments at 250 mg/l and 1,000 mg/l significantly reduced the number of nodules, but rhizobia infection and the overall nitrogenase activity were not affected. Our results show that graphene can be used as a potential vehicle for seed/root treatment.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/aem.01219-22
