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The emergence of commensalism and mutualism often derives from ancestral parasitism. However, in the case of rhizobium-legume interactions, bacterial strains displaying both pathogenic and nodulation features on a single host have not been described yet. Here, we isolated such a bacterium from Medicago nodules. On the same plant genotypes, the T4 strain can induce ineffective nodules in a highly competitive way and behave as a harsh parasite triggering plant death. The T4 strain presents this dual ability on multiple legume species of the Inverted Repeat-Lacking Clade, the output of the interaction relying on the developmental stage of the plant. Genomic and phenotypic clustering analysis show that T4 belongs to the nonsymbiotic Ensifer adhaerens group and clusters together with T173, another strain harboring this dual ability. In this work, we identify a bacterial clade that includes rhizobial strains displaying both pathogenic and nodulating abilities on a single legume host.

Legume-rhizobium symbiosis provides a sustainable nitrogen source for agriculture. Nitrogen fixation efficiency depends on both legume and rhizobium genotypes, but the implications of their interactions for plant performance in environments with many competing rhizobium strains remain unclear. Here, we let 399 Rhizobium leguminosarum complex sv. viciae strains compete for nodulation of 212 faba bean genotypes. We find that the strains can be categorised by their nodule occupancy profiles into groups that show distinct competitive interactions and plant growth-promoting effects. Further, we show that the diversity of strains occupying root nodules affects plant growth and is under plant genetic control. These insights provide a basis for re-designing rhizobium inoculation and plant breeding strategies to enhance symbiotic nitrogen fixation in agriculture. Optimising plant-rhizobium interactions can enhance nitrogen fixation, improving sustainability in agriculture. This study identified four groups of faba bean symbionts that show growth-promoting characteristics and whose diversity across root nodules is under plant genetic control.

Rhizobium leguminosarum bv. viciae mutants unable to transport branched-chain amino acids via the two main amino acid ABC transport complexes AapJQMP and BraDEFGC produce a nitrogen starvation phenotype when inoculated on pea (Pisum sativum) plants [1], [2]. Bacteroids in indeterminate pea nodules have reduced abundance and a lower chromosome number. They reduce transcription of pathways for branched-chain amino acid biosynthesis and become dependent on their provision by the host. This has been called \"symbiotic auxotrophy\". A region important in solute specificity was identified in AapQ and changing P144D in this region reduced branched-chain amino acid transport to a very low rate. Strains carrying P144D were still fully effective for N(2) fixation on peas demonstrating that a low rate of branched amino acid transport in R. leguminosarum bv. viciae supports wild-type rates of nitrogen fixation. The importance of branched-chain amino acid transport was then examined in other legume-Rhizobium symbioses. An aap bra mutant of R. leguminosarum bv. phaseoli also showed nitrogen starvation symptoms when inoculated on French bean (Phaseolus vulgaris), a plant producing determinate nodules. The phenotype is different from that observed on pea and is accompanied by reduced nodule numbers and nitrogen fixation per nodule. However, an aap bra double mutant of Sinorhizobium meliloti 2011 showed no phenotype on alfalfa (Medicago sativa). Symbiotic auxotrophy occurs in both determinate pea and indeterminate bean nodules demonstrating its importance for bacteroid formation and nodule function in legumes with different developmental programmes. However, only small quantities of branched chain amino acids are needed and symbiotic auxotrophy did not occur in the Sinorhizobium meliloti-alfalfa symbiosis under the conditions measured. The contrasting symbiotic phenotypes of aap bra mutants inoculated on different legumes probably reflects altered timing of amino acid availability, development of symbiotic auxotrophy and nodule developmental programmes.

Most species in the Leguminosae (legume family) can fix atmospheric nitrogen (N₂) via symbiotic bacteria (rhizobia) in root nodules. Here, the literature on legume-rhizobia symbioses in field soils was reviewed and genotypically characterised rhizobia related to the taxonomy of the legumes from which they were isolated. The Leguminosae was divided into three sub-families, the Caesalpinioideae, Mimosoideae and Papilionoideae. Bradyrhizobium spp. were the exclusive rhizobial symbionts of species in the Caesalpinioideae, but data are limited. Generally, a range of rhizobia genera nodulated legume species across the two Mimosoideae tribes Ingeae and Mimoseae, but Mimosa spp. show specificity towards Burkholderia in central and southern Brazil, Rhizobium/Ensifer in central Mexico and Cupriavidus in southern Uruguay. These specific symbioses are likely to be at least in part related to the relative occurrence of the potential symbionts in soils of the different regions. Generally, Papilionoideae species were promiscuous in relation to rhizobial symbionts, but specificity for rhizobial genus appears to hold at the tribe level for the Fabeae (Rhizobium), the genus level for Cytisus (Bradyrhizobium), Lupinus (Bradyrhizobium) and the New Zealand native Sophora spp. (Mesorhizobium) and species level for Cicer arietinum (Mesorhizobium), Listia bainesii (Methylobacterium) and Listia angolensis (Microvirga). Specificity for rhizobial species/symbiovar appears to hold for Galega officinalis (Neorhizobium galegeae sv. officinalis), Galega orientalis (Neorhizobium galegeae sv. orientalis), Hedysarum coronarium (Rhizobium sullae), Medicago laciniata (Ensifer meliloti sv. medicaginis), Medicago rigiduloides (Ensifer meliloti sv. rigiduloides) and Trifolium ambiguum (Rhizobium leguminosarum sv. trifolii). Lateral gene transfer of specific symbiosis genes within rhizobial genera is an important mechanism allowing legumes to form symbioses with rhizobia adapted to particular soils. Strain-specific legume rhizobia symbioses can develop in particular habitats.

Nitrogen (N 2 ) fixation in oligotrophic surface waters is the main source of new nitrogen to the ocean 1 and has a key role in fuelling the biological carbon pump 2 . Oceanic N 2 fixation has been attributed almost exclusively to cyanobacteria, even though genes encoding nitrogenase, the enzyme that fixes N 2 into ammonia, are widespread among marine bacteria and archaea 3 – 5 . Little is known about these non-cyanobacterial N 2 fixers, and direct proof that they can fix nitrogen in the ocean has so far been lacking. Here we report the discovery of a non-cyanobacterial N 2 -fixing symbiont, ‘ Candidatus Tectiglobus diatomicola’, which provides its diatom host with fixed nitrogen in return for photosynthetic carbon. The N 2 -fixing symbiont belongs to the order Rhizobiales and its association with a unicellular diatom expands the known hosts for this order beyond the well-known N 2 -fixing rhizobia–legume symbioses on land 6 . Our results show that the rhizobia–diatom symbioses can contribute as much fixed nitrogen as can cyanobacterial N 2 fixers in the tropical North Atlantic, and that they might be responsible for N 2 fixation in the vast regions of the ocean in which cyanobacteria are too rare to account for the measured rates. A symbiosis between a diatom and a newly discovered species of alphaproteobacteria, ‘ Candidatus Tectiglobus diatomicola’, can fix nitrogen in the ocean, providing evidence that nitrogen fixers other than cyanobacteria have a key role in the marine environment.

Drought is one of the most serious abiotic stresses, and emerging evidence suggest plant microbiome affects plant drought tolerance. However, there is a lack of genetic evidence regarding whether and how plants orchestrate the dynamic assembly of the microbiome upon drought. By utilizing mutants with enhanced or decreased root hair densities, we find that root hair regulators also affect drought induced root microbiome changes. Rhizobiaceae is a key biomarker taxa affected by root hair related mutants. We isolated and sequenced 1479 root associated microbes, and confirmed that several Rhizobium strains presented stress-alleviating activities. Metagenome, root transcriptome and root metabolome studies further reveal the multi-omic changes upon drought stress. We knocked out an ornithine cyclodeaminase ( ocd ) gene in Rhizobium sp. 4F10, which significantly dampens its stress alleviating ability. Our genetic and integrated multi-omics studies confirm the involvement of host genetic effects in reshaping a stress-alleviating root microbiome during drought, and provide mechanistic insights into Rhizobiaceae mediated abiotic stress protection. Plant microbiome confers fitness benefits upon drought. By integrating plant genetic, microbial genetic and multi-omics approaches, this work reveals the critical role of root hair developmental regulators in shaping drought alleviating microbiome.

Rhizobia are some of the best-studied plant microbiota. These oligotrophic Alphaproteobacteria or Betaproteobacteria form symbioses with their legume hosts. Rhizobia must exist in soil and compete with other members of the microbiota before infecting legumes and forming N2 -fixing bacteroids. These dramatic lifestyle and developmental changes are underpinned by large genomes and even more complex pan-genomes, which encompass the whole population and are subject to rapid genetic exchange. The ability to respond to plant signals and chemoattractants and to colonize nutrient-rich roots are crucial for the competitive success of these bacteria. The availability of a large body of genomic, physiological, biochemical and ecological studies makes rhizobia unique models for investigating community interactions and plant colonization.

Human activities have altered the global nitrogen (N) cycle, and as a result, elevated N inputs are causing profound ecological changes in diverse ecosystems. The evolutionary consequences of this global change have been largely ignored even though elevated N inputs are predicted to cause mutualism breakdown and the evolution of decreased cooperation between resource mutualists. Using a long-term (22 years) N-addition experiment, we find that elevated N inputs have altered the legume–rhizobium mutualism (where rhizobial bacteria trade N in exchange for photosynthates from legumes), causing the evolution of less-mutualistic rhizobia. Plants inoculated with rhizobium strains isolated from N-fertilized treatments produced 17–30% less biomass and had reduced chlorophyll content compared to plants inoculated with strains from unfertilized control plots. Because the legume–rhizobium mutualism is the major contributor of naturally fixed N to terrestrial ecosystems, the evolution of less-cooperative rhizobia may have important environmental consequences.

Legumes are high in protein and form a valuable part of human diets due to their interaction with symbiotic nitrogen-fixing bacteria known as rhizobia. Plants house rhizobia in specialized root nodules and provide the rhizobia with carbon in return for nitrogen. However, plants usually housemultiple rhizobial strains that vary in their fixation ability, so the plant faces an investment dilemma. Plants are known to sanction strains that do not fix nitrogen, but nonfixers are rare in field settings, while intermediate fixers are common. Here, we modeled how plants should respond to an intermediate fixer that was otherwise isogenic and tested model predictions using pea plants. Intermediate fixers were only tolerated when a better strain was not available. In agreement with model predictions, nodules containing the intermediate-fixing strain were large and healthy when the only alternative was a nonfixer, but nodules of the intermediate-fixing strain were small and white when the plant was coinoculated with a more effective strain. The reduction in nodule size was preceded by a lower carbon supply to the nodule even before differences in nodule size could be observed. Sanctioned nodules had reduced rates of nitrogen fixation, and in later developmental stages, sanctioned nodules contained fewer viable bacteria than nonsanctioned nodules. This indicates that legumes can make conditional decisions, most likely by comparing a local nodule-dependent cue of nitrogen output with a global cue, giving them remarkable control over their symbiotic partners.

Pea and vetch are the important legume crops used as food, forage, and green manure in agriculture. Several new rhizobial isolates were obtained from vetch Vicia sativa root nodules. For one of them, Vst36-3, the nodulation test showed various specificity in relation to plant hosts from the Fabeae tribe, such as pea and vetch. It is in contrast to typical strains of the Rhizobium leguminosarum species complex (Rlc), which formed effective nodules as in pea and vetch. Here, whole genome sequencing was performed followed by de novo genome assembly for Vst36-3 strain. As a result of de novo genome assembly, seven contigs were generated using Oxford Nanopore Technology long reads and subsequently Illumina short reads. Phylogenetic analysis allowed us to identify this strain as Rhizobium ruizarguesonis Vst36-3. Analysis of the Sym plasmid containing the nod and nif genes revealed that R. ruizarguesonis Vst36-3 has a complete suite of essential genes for the development of symbiosis. Nevertheless, this new strain forms ineffective nodules in pea. This makes Rhizobium ruizarguesonis Vst36-3 attractive for the search and investigation of new factors of host specificity in future.