Long-term microclimatic stress causes rapid adaptive radiation of kaiABC clock gene family in a cyanobacterium, Nostoc linckia, from “Evolution Canyons” I and II, Israel

Cyanobacteria are the only prokaryotes known thus far possessing regulation of physiological functions with approximate daily periodicity, or circadian rhythms, that are controlled by a cluster of three genes, kaiA, kaiB, and kaiC. Here we demonstrate considerably higher genetic polymorphism and extremely rapid evolution of the kaiABC gene family in a filamentous cyanobacterium, Nostoc linckia, permanently exposed to the acute natural environmental stress in the two microsite evolutionary models known as “Evolution Canyons,” I (Mount Carmel) and II (Upper Galilee) in Israel. The family consists of five distinct subfamilies (kaiI–kaiV) comprising at least 20 functional genes and pseudogenes. The obtained data suggest that the duplications of kai genes have adaptive significance, and some of them are evolutionarily quite recent (≈80,000 years ago). The observed patterns of within- and between-subfamily polymorphisms indicate that positive diversifying, balancing, and purifying selections are the principal driving forces of the kai gene family's evolution.