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1. Interspecific conflict and the evolution of ineffective rhizobia

   https://doi.org/10.1111/ele.13247  

   Gano‐Cohen, Kelsey A.; Wendlandt, Camille E.; Stokes, Peter J.; Blanton, Mia A.; Quides, Kenjiro W.; Zomorrodian, Avissa; Adinata, Eunice S.; Sachs, Joel L.; Johnson, ed., Nancy (March 2019, Ecology Letters)

   Abstract 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 formingBradyrhizobiumsymbionts inAcmisponhosts. We uncoveredBradyrhizobiumgenotypes that provide negligible mutualist services to hosts and had superiorin plantafitness 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 byBradyrhizobiumgenotypes 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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2. Spontaneously Produced Lysogenic Phages Are an Important Component of the Soybean Bradyrhizobium Mobilome

   https://doi.org/10.1128/mbio.00295-23  

   Joglekar, Prasanna; Ferrell, Barbra D.; Jarvis, Tessa; Haramoto, Kona; Place, Nicole; Dums, Jacob T.; Polson, Shawn W.; Wommack, K. Eric; Fuhrmann, Jeffry J. (April 2023, mBio)

   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. 

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3. Recurrent mutualism breakdown events in a legume rhizobia metapopulation

   https://doi.org/10.1098/rspb.2019.2549  

   Gano-Cohen, Kelsey A.; Wendlandt, Camille E.; Al Moussawi, Khadija; Stokes, Peter J.; Quides, Kenjiro W.; Weisberg, Alexandra J.; Chang, Jeff. H.; Sachs, Joel L. (January 2020, Proceedings of the Royal Society B: Biological Sciences)

   Bacterial mutualists generate major fitness benefits for eukaryotes, reshaping the host phenotype and its interactions with the environment. Yet, microbial mutualist populations are predicted to generate mutants that defect from providing costly services to hosts while maintaining the capacity to exploit host resources. Here, we examined the mutualist service of symbiotic nitrogen fixation in a metapopulation of root-nodulating Bradyrhizobium spp . that associate with the native legume Acmispon strigosus . We quantified mutualism traits of 85 Bradyrhizobium isolates gathered from a 700 km transect in California spanning 10 sampled A. strigosus populations. We clonally inoculated each Bradyrhizobium isolate onto A. strigosus hosts and quantified nodulation capacity and net effects of infection, including host growth and isotopic nitrogen concentration. Six Bradyrhizobium isolates from five populations were categorized as ineffective because they formed nodules but did not enhance host growth via nitrogen fixation. Six additional isolates from three populations failed to form root nodules. Phylogenetic reconstruction inferred two types of mutualism breakdown, including three to four independent losses of effectiveness and five losses of nodulation capacity on A. strigosus . The evolutionary and genomic drivers of these mutualism breakdown events remain poorly understood. 

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4. Metabolomic profiling of wild‐type and mutant soybean root nodules using laser‐ablation electrospray ionization mass spectrometry reveals altered metabolism

   https://doi.org/10.1111/tpj.14815  

   Agtuca, Beverly J.; Stopka, Sylwia A.; Evans, Sterling; Samarah, Laith; Liu, Yang; Xu, Dong; Stacey, Minviluz G.; Koppenaal, David W.; Paša‐Tolić, Ljiljana; Anderton, Christopher R.; et al (June 2020, The Plant Journal)

   SUMMARY The establishment of the nitrogen‐fixing symbiosis between soybean andBradyrhizobium japonicumis a complex process. To document the changes in plant metabolism as a result of symbiosis, we utilized laser ablation electrospray ionization‐mass spectrometry (LAESI‐MS) forin situmetabolic profiling of wild‐type nodules, nodules infected with aB. japonicum nifHmutant unable to fix nitrogen, nodules doubly infected by both strains, and nodules formed on plants mutated in thestearoyl‐acyl carrier protein desaturase(sacpd‐c) gene, which were previously shown to have an altered nodule ultrastructure. The results showed that the relative abundance of fatty acids, purines, and lipids was significantly changed in response to the symbiosis. ThenifHmutant nodules had elevated levels of jasmonic acid, correlating with signs of nitrogen deprivation. Nodules resulting from the mixed inoculant displayed similar, overlapping metabolic distributions within the sectors of effective (fix⁺) and ineffective (nifHmutant, fix⁻) endosymbionts. These data are inconsistent with the notion that plant sanctioning is cell autonomous. Nodules lackingsacpd‐cdisplayed an elevation of soyasaponins and organic acids in the central necrotic regions. The present study demonstrates the utility of LAESI‐MS for high‐throughput screening of plant phenotypes. Overall, nodules disrupted in the symbiosis were elevated in metabolites related to plant defense. 

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5. Surface Properties and Adherence of Bradyrhizobium diazoefficiens to Glycine max Roots Are Altered When Grown in Soil Extracted Nutrients

   https://doi.org/10.3390/nitrogen2040031  

   Sandhu, Armaan Kaur; Subramanian, Senthil; Brözel, Volker S. (December 2021, Nitrogen)

   Soybean roots are colonized and nodulated by multiple strains of compatible nitrogen-fixing rhizobia primarily belonging to the Genus Bradyrhizobium. Motility towards the root and attachment to root hairs are key determinants of competitive colonization and subsequent nodulation. Bacterial surface properties and motility are known to vary with chemical composition of the culture medium, and root adhesion and nodulation occur in a soil environment rather than laboratory medium. We asked whether the nodulation-promoting factors motility, surface hydrophobicity and surface adhesion of Bradyrhizobium are affected by growth in a soil nutrient environment. B. diazoefficiens USDA 110, 126, 3384, and B. elkanii USDA 26 were grown in mineral salt medium with peptone, yeast extract and arabinose (PSY), and in a soil extracted soluble organic matter (SESOM) medium. Surface hydrophobicity was determined by partitioning into hydrocarbon, motility by transition through soft agar, and surface-exposed saccharides by lectin profiling, followed by biofilm formation and soybean root adhesion capacity of populations. SESOM-grown populations were generally less motile and more hydrophobic. They bound fewer lectins than PSY-grown populations, indicating a simpler surface saccharide profile. SESOM populations of USDA 110 did not form detectable biofilm, but showed increased binding to soy roots. Our results indicate that growth in a soil environment impacts surface properties, motility, and subsequent soy root adhesion propensity. Hence, evaluation of Bradyrhizobium for nodulation efficiency should be performed using soil from the specific field where the soybeans are to be planted, rather than laboratory culture media. 

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