title: Expanding the Limits of Thermoacidophily in the Archaeon Sulfolobus solfataricus by Adaptive Evolution.
abstract: Extremely thermoacidophilic Crenarchaeota belonging to the order Sulfolobales flourish in hot acidic habitats that are strongly oxidizing. The pH extremes of these habitats, however, often exceed the acid tolerance of type species and strains. Here, adaptive laboratory evolution was used over a 3-year period to test whether such organisms harbor additional thermoacidophilic capacity. Three distinct cell lines derived from a single type species were subjected to high-temperature serial passage while culture acidity was gradually increased. A 178-fold increase in thermoacidophily was achieved after 29 increments of shifted culture pH resulting in growth at pH 0.8 and 80°C. These strains were named super-acid-resistant Crenarchaeota (SARC). Mathematical modeling using growth parameters predicted the limits of acid resistance, while genome resequencing and transcriptome resequencing were conducted for insight into mechanisms responsible for the evolved trait. Among the mutations that were detected, a set of eight nonsynonymous changes may explain the heritability of increased acid resistance despite an unexpected lack of transposition. Four multigene components of the SARC transcriptome implicated oxidative stress as a primary challenge accompanying growth at acid extremes. These components included accelerated membrane biogenesis, induction of the mer operon, and an increased capacity for the generation of energy and reductant.
authors.affiliation: School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, USA.
authors.forename: Samuel
authors.initials: S
authors.lastname: McCarthy
authors.affiliation: School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, USA.
authors.forename: Tyler
authors.initials: T
authors.lastname: Johnson
authors.affiliation: Department of Chemical and Biomolecular Engineering, University of Nebraska-Lincoln, Lincoln, Nebraska, USA.
authors.forename: Benjamin J
authors.initials: BJ
authors.lastname: Pavlik
authors.affiliation: School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, USA.
authors.forename: Sophie
authors.initials: S
authors.lastname: Payne
authors.affiliation: U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, USA.
authors.forename: Wendy
authors.initials: W
authors.lastname: Schackwitz
authors.affiliation: U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, USA.
authors.forename: Joel
authors.initials: J
authors.lastname: Martin
authors.affiliation: U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, USA.
authors.forename: Anna
authors.initials: A
authors.lastname: Lipzen
authors.affiliation: School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, USA.
authors.forename: Erica
authors.initials: E
authors.lastname: Keffeler
authors.affiliation: School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, USA Department of Chemical and Biomolecular Engineering, University of Nebraska-Lincoln, Lincoln, Nebraska, USA pblum1@unl.edu.
authors.forename: Paul
authors.initials: P
authors.lastname: Blum
mesh_terms: D000222:Adaptation, Physiological; D019843:Archaeal Proteins / Q000235:genetics / Q000378:metabolism; D001709:Biotechnology; D019020:Directed Molecular Evolution; D016680:Genome, Bacterial; D006358:Hot Temperature; D006863:Hydrogen-Ion Concentration; D008954:Models, Biological; D005810:Multigene Family; D009154:Mutation; D009876:Operon; D010084:Oxidation-Reduction; D018384:Oxidative Stress / Q000235:genetics; D017422:Sequence Analysis, DNA; D048229:Sulfolobus solfataricus / Q000235:genetics* / Q000254:growth & development / Q000502:physiology*; D013997:Time Factors; D059467:Transcriptome
chemical_list: D019843:Archaeal Proteins