Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont

Abstract

Cyanobacteria belonging to the genus Nostoc comprise free-living strains and also facultative plant symbionts. Symbiotic strains can enter into symbiosis with taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here, we compared the genomes derived from 11 symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic clade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, and inference of transfer events implied that this trait was likely acquired several times in the evolution of the Nostocales. Symbiotic Nostoc strains showed enriched functions in transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, branched-chain amino acids, and ammonium. The genomes of the intracellular clade differ from that of other Nostoc strains, with a gain/enrichment of genes encoding proteins to generate l-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromolecule xylan present in plant cell walls. These compounds could function as C-sources for members of the intracellular clade. Molecular clock analysis indicated that the intracellular clade emerged ca. 600 Ma, suggesting that intracellular Nostoc symbioses predate the origin of land plants and the emergence of their extant hosts.

Cycad coralloid roots contain bacterial communities including cyanobacteria andCaulobacterspp that encode niche-specific biosynthetic gene clusters

“…To confirm the presence of diazotrophic organisms in our sub-community co-cultures, we searched for the NifH protein sequence, an enzyme involved in nitrogen fixation and relevant in symbiotic relationships (Warshan et al 2018). We used the NifH protein from Nostoc punctiforme PCC 73102 (B2IV87), Bradyrhizobium japonicum OX=375 (I4DDG5) and Mesorhizobium japonicum LMG 29417 (Q98AP7) from the NCBI databases (July 2018).…”

“…Likewise, RF15115 from D. merolae, with 33k59, 35k25 and 3335mG from D. edule, form a monophyletic clade with Nostoc punctiforme PCC 73102 from the cycad Macrozamia and Nostoc sp. KVJ20 from the liverwort Blasia pusilla (Warshan et al 2018).…”

“…Likewise, various chemical, physical and physiological processes appear to regulate the cycad-bacteria interaction (Lobakova et al 2003a, Meeks 2009), although genes coding for these specialized mechanisms of the symbiosis have been not identified. The presence of unique specialized metabolites in the cycad coralloid root bacterial endophytes is of interest to us because they may be a result of co-evolution between the cycad host and the endophyte bacterial community (Scherlach, et al 2018, Warshan et al 2018.…”

“…Certain soil-dwelling and aquatic bacteria, including cyanobacteria, have genomic plasticity (Warshan, et al, 2018) and the capacity to synthesize specialized metabolites with overwhelming chemical diversity, believed to be produced to cope with biotic and abiotic pressures. These bacterial traits are concomitant with large genomes that code for specialized metabolites in rapidly evolving genetic units called biosynthetic gene clusters (BGCs) of about 25-40 Kbp (Tan, 2007).…”

The nitrogen-fixing symbiotic cyanobacterium,Nostoc punctiformecan regulate plant programmed cell death

“…likely evolved from a single common ancestor, whereas extracellular plant-symbiotic species likely evolved convergently (Warshan et al, 2017(Warshan et al, , 2018. This suggests that Nostoc cyanobionts may possess specialised suites of genes which immunologically permit symbiotic association.…”