Horizontal Transfer of Symbiosis Genes within and Between Rhizobial Genera: Occurrence and Importance

Abstract

Rhizobial symbiosis genes are often carried on symbiotic islands or plasmids that can be transferred (horizontal transfer) between different bacterial species. Symbiosis genes involved in horizontal transfer have different phylogenies with respect to the core genome of their ‘host’. Here, the literature on legume⁻rhizobium symbioses in field soils was reviewed, and cases of phylogenetic incongruence between rhizobium core and symbiosis genes were collated. The occurrence and importance of horizontal transfer of rhizobial symbiosis genes within and between bacterial genera were assessed. Horizontal transfer of symbiosis genes between rhizobial strains is of common occurrence, is widespread geographically, is not restricted to specific rhizobial genera, and occurs within and between rhizobial genera. The transfer of symbiosis genes to bacteria adapted to local soil conditions can allow these bacteria to become rhizobial symbionts of previously incompatible legumes growing in these soils. This, in turn, will have consequences for the growth, life history, and biogeography of the legume species involved, which provides a critical ecological link connecting the horizontal transfer of symbiosis genes between rhizobial bacteria in the soil to the above-ground floral biodiversity and vegetation community structure.

Keywords: Fabaceae; N2 fixation; lateral gene transfer; legumes; nod genes; nodulation.

Figure 1

Comparative maximum likelihood phylogenetic analysis using housekeeping and symbiotic gene clusters from Mesorhizobium strains isolated from New Zealand endemic Sophora spp. Sequence alignment, alignment editing, and phylogenetic analysis were performed using MEGA7 [24]. The phylogenetic trees were built using the GTR model with G + I substitutions for the housekeeping genes (1083 bp) and Tamura 3-parameter model with G + I substitutions for the symbiosis genes (869 bp). The possibility of concatenation was investigated using the partition-homogeneity test with PAUP [25,26]. Each concatenation was investigated for 1000 replicates. All housekeeping genes were congruent with each other (p = 0.015), and both symbiosis genes were congruent with each other (p = 0.02). The housekeeping genes were shown not to be congruent with the symbiosis genes (p = 0.001). Bootstrap values after 500 replicates are expressed as percentages; values less than 50% are not shown. The scale bar indicates the fraction of substitutions per site. M: Mesorhizobium, S: Sophora, FS: Field Site.

Figure 2

Recombination and circularization of Mesorhizobium loti R7A integrative and conjugative elements (ICEMlSym^R7A) [20,119,120,121]. The recombination is initiated by IntS (integration factor S) at the attachment sites attB and attP to integrate the ICEMlSym^R7A in the chromosome and produce the attachment sites attL and attR. The recombination directionality factor S (RdfS) together with IntS stimulates excision of the ICE and forms the attachment sites attP and attB. phe-tRNA = phenylalanine transfer RNA. The ICEMlSym^R7A is coloured blue, and the remaining chromosome is coloured grey. The schematic diagram is not drawn to scale.

Figure 3

Comparative genome analysis using the circular BLASTN alignment in BRIG (BLAST Ring Image Generator, [124] of WSM2073 and WSM2075 against WSM1271. The three ICEMcSym¹²⁷¹ regions are indicated and summarised from Haskett et al. [123]. It highlights the transfer of the symbiosis island from the Biserrula pelecinus inoculant strain WSM1271 to non-symbiotic recipient strains that turn into poorly effective symbionts. ICEMcSym¹²⁷¹ consists of three separate regions (alpha, beta, and gamma) when integrated in the chromosome but excises as one circular plasmid and re-integrates in the recipient chromosome [123].