Lupin, a Unique Legume That Is Nodulated by Multiple Microsymbionts: The Role of Horizontal Gene Transfer

Abstract

Lupin is a high-protein legume crop that grows in a wide range of edaphoclimatic conditions where other crops are not viable. Its unique seed nutrient profile can promote health benefits, and it has been proposed as a phytoremediation plant. Most rhizobia nodulating Lupinus species belong to the genus Bradyrhizobium, comprising strains that are phylogenetically related to B. cytisi, B. hipponenese, B. rifense, B. iriomotense/B. stylosanthis, B. diazoefficiens, B. japonicum, B. canariense/B. lupini, and B. retamae/B. valentinum. Lupins are also nodulated by fast-growing bacteria within the genera Microvirga, Ochrobactrum, Devosia, Phyllobacterium, Agrobacterium, Rhizobium, and Neorhizobium. Phylogenetic analyses of the nod and nif genes, involved in microbial colonization and symbiotic nitrogen fixation, respectively, suggest that fast-growing lupin-nodulating bacteria have acquired their symbiotic genes from rhizobial genera other than Bradyrhizobium. Horizontal transfer represents a key mechanism allowing lupin to form symbioses with bacteria that were previously considered as non-symbiotic or unable to nodulate lupin, which might favor lupin’s adaptation to specific habitats. The characterization of yet-unstudied Lupinus species, including microsymbiont whole genome analyses, will most likely expand and modify the current lupin microsymbiont taxonomy, and provide additional knowledge that might help to further increase lupin’s adaptability to marginal soils and climates.

Adaptation to mercury stress by nitrogen-fixing bacteria is driven by horizontal gene transfer and enhanced gene expression of the Mer operon

“…Recently, it has been shown that varying degrees of metal stress in the local population may increase the frequency of HGT events [23], providing a source of adaptive evolution in bacteria [22] in contaminated environments. Moreover, HGT is also crucial in rhizobia to determine their host range [77]. And while we typically expect selection to act on standing genetic variation in a species [78], the mechanism of HGT can cross species boundaries, accelerating adaptation, even if the donor genetic locus is at low frequency in the population [79] or in the microbiome of the rhizosphere.…”

Local adaptation to mercury contamination by nitrogen-fixing rhizobia is driven by horizontal gene transfer, copy number, and enhanced gene expression

“…Recently, it has been shown that varying degrees of metal stress in the local population may increase the frequency of HGT events (Chen et al, 2023), providing a source of adaptive evolution in bacteria (Arnold et al, 2022) in contaminated environments. Moreover, HGT is also crucial in rhizobia to determine their host range (Msaddak et al, 2023). And while we typically expect selection to act on standing genetic variation in a species (Barrett and Schluter, 2008), the mechanism of HGT can cross species boundaries, accelerating adaptation, even if the donor genetic locus is at low frequency in the population (Woods et al, 2020) or in the microbiome of the rhizosphere.…”

The Beneficial Effects of Inoculation with Selected Nodule-Associated PGPR on White Lupin Are Comparable to Those of Inoculation with Symbiotic Rhizobia

“…Furthermore, these described mechanisms render white lupin a suitably adapted plant for acidic soil conditions impacted by aluminum toxicity [ 8 ]. Its capacity to thrive in environments with low nutrient content, acidity, or moderate pollution levels, as well as in both dry and cold climates, allows this legume to grow in a wide range of edaphoclimatic conditions [ 1 , 9 ].…”