Niche adaptation by expansion and reprogramming of general transcription factors

Numerous lineage‐specific expansions of the transcription factor B (TFB) family in archaea suggests an important role for expanded TFBs in encoding environment‐specific gene regulatory programs. Given the characteristics of hypersaline lakes, the unusually large numbers of TFBs in halophilic archaea further suggests that they might be especially important in rapid adaptation to the challenges of a dynamically changing environment. Motivated by these observations, we have investigated the implications of TFB expansions by correlating sequence variations, regulation, and physical interactions of all seven TFBs in Halobacterium salinarum NRC‐1 to their fitness landscapes, functional hierarchies, and genetic interactions across 2488 experiments covering combinatorial variations in salt, pH, temperature, and Cu stress. This systems analysis has revealed an elegant scheme in which completely novel fitness landscapes are generated by gene conversion events that introduce subtle changes to the regulation or physical interactions of duplicated TFBs. Based on these insights, we have introduced a synthetically redesigned TFB and altered the regulation of existing TFBs to illustrate how archaea can rapidly generate novel phenotypes by simply reprogramming their TFB regulatory network. Experimental analysis of TFB family proteins in a halophilic archaeon reveals complex environment‐dependent fitness contributions. Gene conversion events among these proteins can generate novel niche adaptation capabilities, a process that may have contributed to archaeal adaptation to extreme environments. Synopsis Experimental analysis of TFB family proteins in a halophilic archaeon reveals complex environment‐dependent fitness contributions. Gene conversion events among these proteins can generate novel niche adaptation capabilities, a process that may have contributed to archaeal adaptation to extreme environments. The evolutionary success of an organism depends on its ability to continually adapt to changes in the patterns of constant, periodic, and transient challenges within its environment. This process of ‘niche adaptation’ requires reprogramming of the organism's environmental response networks by reorganizing interactions among diverse parts including environmental sensors, signal transducers, and transcriptional and post‐transcriptional regulators. Gene duplications have been discovered to be one of the principal strategies in this process, especially for reprogramming of gen