Diverse fates of ancient horizontal gene transfers in extremophilic red algae
Julia Van Etten, Timothy G. Stephens, Erin Chille, Anna Lipzen, Daniel Peterson, Kerrie Barry, Igor V. Grigoriev and Debashish Bhattacharya
Graduate Program in Ecology and Evolution, Rutgers, The State University of New Jersey, New Brunswick, NJ 08901, United States of America

Horizontal genetic transfer (HGT) is widespread in eukaryotic genomes, yet, how HGTs persist and may be integrated into other pathways is poorly understood. This aspect is of high interest because, over time, stressors that initially favored HGT fixation may diminish or disappear, yet the foreign gene(s) may survive if they are integrated into a broader stress (or other) response. The standard model, whereby HGT acquisition equals adaptation, may thereby evolve into more complex gene product interactions which we refer to as the “integrated HGT model” (IHM). We address this latter outcome by studying specialized HGT-derived genes encoding heavy metal detoxification functions, whose recruitment into other pathways is easier to interpret as cases of IHM. Using lab cultures, two anciently diverged species of polyextremophilic red algae in the genus Galdieria were exposed to arsenic and mercury stress and transcriptome data were analyzed using differential and co-expression analysis. We found that mercury detoxification is a one gene-one function, indivisible response, whereas arsH in the arsenite response pathway shows a complex pattern of duplication, divergence, and putative neofunctionalization consistent with the IHM. Our work elucidates the fate and integration of ancient HGTs, providing a novel perspective on the ecology of extremophiles.