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Rhizobial Communities in Symbiosis with Legumes: Genetic Diversity, Competition and Interactions with Host Plants

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Rhizobial Communities in Symbiosis with Legumes: Genetic Diversity, Competition and Interactions with Host Plants Cent. Eur. J. Biol. • 7(3) • 2012 • 363-372 DOI: 10.2478/s11535-012-0032-5 Central European Journal of Biology Rhizobial communities in symbiosis with legumes: genetic diversity, competition and interactions with host plants Review Article Jerzy Wielbo* Department of Genetics and Microbiology, Maria Curie-Skłodowska University, 20-033 Lublin, Poland Received 01 December 2011; Accepted 28 February 2012 Abstract: The term `Rhizobium-legume symbiosis’ refers to numerous plant-bacterial interrelationships. Typically, from an evolutionary perspective, these symbioses can be considered as species-to-species interactions, however, such plant-bacterial symbiosis may also be viewed as a low-scale environmental interplay between individual plants and the local microbial population. Rhizobium-legume interactions are therefore highly important in terms of microbial diversity and environmental adaptation thereby shaping the evolution of plant-bacterial symbiotic systems. Herein, the mechanisms underlying and modulating the diversity of rhizobial populations are presented. The roles of several factors impacting successful persistence of strains in rhizobial populations are discussed, shedding light on the complexity of rhizobial-legume interactions. Keywords: Symbiotic nitrogen fixation • Rhizobia • Bacterial populations • Genetic diversity • Strain competition © Versita Sp. z o.o. 1. Rhizobia and their role in biological belong to α-proteobacterial genera Azorhizobium, Allorhizobium, Bradyrhizobium, Mesorhizobium, nitrogen fixation Rhizobium, Sinorhizobium (Ensifer), Devosia, The most efficient biological nitrogen fixation (BNF) is Methylobacterium, Ochrobactrum and Phyllobacterium, conducted in symbiotic systems comprising bacterial whereas some, including Burkholderia and Cupriavidus, microsymbionts collectively known as rhizobia and plant are members of β-proteobacteria [5-8]. Rhizobia are soil hosts belonging to Leguminoseae family. Total global microorganisms which are phylogenetically, genetically BNF is estimated at 100-300 Tg N per annum, and the and metabolically diverse, however, all of them can amount of N2 derived from rhizobial-legume symbioses elicit the formation of root or, occasionally, stem nodules (50-70 Tg N per annum) is comparable with the total – i.e. new and specific plant outgrowths where dinitrogen- amount of N fixed industrially in fertilizer production to-ammonia reduction occurs. In contrast to other (80–90 Tg N per annum) [1,2]. Even though crop, diazotrophs (such as plant-associated Azospirillum), pasture and wild legumes assimilate and accumulate rhizobial-legume symbioses are species-specific – for BNF-derived nitrogen to differing levels [3], in most instance, Rhizobium leguminosarum bv. trifolii can cases, symbiotically reduced N2 covers more than half colonize the nodules of clovers (Trifolium spp.), whereas of total nitrogen requirements of a plant [2,4]. It is worth R. etli exclusively colonizes bean (Phaseolus vulgaris) noticing that in pulse or pasture legumes 30–60% of nodules [5,9]. In some instances a single plant host may total plant N may be rhizo-deposited [2], and this under- be inhabited by diverse rhizobial species - for example, ground N can be subsequently used by other crops, bean (P. vulgaris) can act as a host for R. etli, R. gallicum emphasizing the agricultural and ecological importance and R tropici, whereas pea (Pisum sativum) can host of rhizobial-legume symbioses. R. leguminosarum bv. viciae, R. pisi and R. fabae Legumes can develop symbiotic interactions with [5,10,11]. Taking into consideration the diversity of many different species of bacteria. Most microsymbionts legumes and rhizobial species, and the specificity * E-mail: [email protected] 363 Rhizobial communities in symbiosis with legumes: genetic diversity, competition and interactions with host plants and host range in plant-microsymbiont interactions, Phylogenetic analysis of repABC sequences enabled a `network of relationships’ between legumes and the investigation of the history of a plasmid set present rhizobial species can be drawn [12]. in specific rhizobial strains and tracing of subsequent The establishment and development of symbiosis events of plasmid acquisition [25-27]. Moreover, some is a multi-step process, involving numerous signaling of the rhizobial plasmids are unique in that they cannot and regulatory pathways. Plant flavonoid-dependent be eliminated from the genome, due to the presence of recognition of compatible symbiotic partners and the genes participating in the primary metabolism, and they induction of nodule formation initiated by rhizobial Nod are sometimes regarded as `secondary chromosomes` factors are followed by the invasion of plant tissues [28]. Some of them are called `chromids` due to their by bacteria [13]. Upon reaching the nodule primordia, mixed (plasmid/chromosome) characteristic: (a) plasmid rhizobia aggregate and participate in the growth and replication and partitioning system with (b) chromosome- development of nodules. As a result, either the entire type nucleotide composition and codon usage, as well nodules mature (in the case of determinate nodules) or as the presence of some `core genome` genes [29]. symbiotic zones of nodules are formed (in indeterminate The `rhizobial core genome’ is not easy to nodules), where the process of BNF is facilitated by define because the former distinction between the bacteria differentiated into bacteroids and living as `essential genetic material` (i.e. chromosome) and endosymbionts inside the plant cells. Simultaneously, the `supplementary genetic material` (i.e. plasmids) is photosynthates (plant-derived carbohydrate not straightforward. Although chromosomes of strains compounds) are exchanged for bacterial-derived are classified into the same species, they may differ nitrogen compounds, and this process continues until substantially with the percentage of unique genes the nodules decay [13-15]. Most of rhizobia inside the reaching up to 40% of the genome [23,30]. Therefore, nodules are converted into bacteroids, however, some the `pan-genome’ concept arose, which assumes that of them remain in vegetative form. These saprophytic the genome of a particular species can be defined only (non-symbiotic) forms of rhizobia are released into the after the analysis of genomes of numerous strains. soil after multiplication in the nodules, thus restoring/ In a pan-genome, three classes of genes should be enriching soil populations of rhizobia [16]. distinguished: `core genes’ (replication, translation, energy homeostasis), `extended core genes’ (adaptation to a defined environmental niche) and `accessory genes’ 2. Rhizobial genomes - a scheme for (all other functions – no size limit on the group). Only the extraordinary strain diversity core and extended core gene sets must be present in all the strains [31]. Rhizobial genomes are large (6–9 Mb) and have complex The application of the pan-genome concept to the architecture, being composed of a chromosome and a available sequenced rhizobial genomes revealed that set of large plasmids [17-19]. In most species, the main the rhizobial core genes are mainly located on the genetic symbiotic component, i.e. genes responsible chromosome, with some genes dispersed between for plant nodulation and nitrogen fixation, is clustered plasmids. Core genes were found on different plasmid on a symbiotic plasmid (pSym). Alternatively, it can replicons, and not only on chromids. They were be incorporated into the chromosome [20]. All of the maintained in syntenic blocks and revealed high level studied rhizobial genomes are redundant and possess of nucleotide identity of homologous segments, also in mosaic structure, i.e. regions with high degree of the case of symbiosis-related genes located on pSyms synteny are separated by other sequences [18,21,22] [30]. Thus, the architecture of rhizobial genomes and Such characteristic genome structure might result the classification of replicons as plasmids/chromids or from numerous genetic transfers and recombinations, symbiotic/nonsymbiotic plasmids seem to be of minor whereas the unusual size and enrichment in the importance [30,32]. regulation, transport and secondary metabolism genes Rhizobial plasmid replicons have less synteny is environmentally advantageous - the rhizobia must be than chromosomes [33], and it is possible that such capable of thriving in completely different environments, mosaic plasmid structure results from frequent genetic soil and plant tissues [23,24]. rearrangements [34]. Moreover, some of them are self- Rhizobial plasmids are extremely interesting due transmissible or can be transferred to other bacterial to their extraordinary size, biological importance as cells in the presence of other plasmids [35,36]. The well as interrelations with other parts of the genome. frequency of plasmid transfer between rhizobial strains Most of them possess repABC operon, a common and the role of this genetic exchange in rhizobial replication-partitioning system in α-proteobacteria. evolution remains controversial [37-40]. However, the 364 J. Wielbo pool of plasmid replicons present in rhizobial cells is effectiveness is not beneficial for rhizobia [58,59], but regarded as a (mostly) accessory genetic component some plant-derived mechanisms selecting effective which is evolving more rapidly than the chromosome microsymbionts have been postulated including the [33], due to frequent changes (such as gene duplication, allocation of greater carbon
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