Expanding the limits of thermoacidophily in the archaeon Sulfolobus solfataricus by adaptive evolution

Samuel McCarthy, Tyler Johnson, Benjamin J. Pavlik, Sophie Payne, Wendy Schackwitz, Joel Martin, Anna Lipzen, Erica Keffeler, Paul H Blum

Research output: Contribution to journalArticle

15 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)857-867
Number of pages11
JournalApplied and environmental microbiology
Volume82
Issue number3
DOIs
StatePublished - Jan 1 2016

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Sulfolobus solfataricus
Crenarchaeota
acid tolerance
Archaea
transcriptome
Acids
acids
acid
reducing agents
transposition (genetics)
operon
habitats
Transcriptome
Sulfolobales
Ecosystem
acidity
heritability
oxidative stress
mathematical models
Growth

ASJC Scopus subject areas

  • Biotechnology
  • Food Science
  • Applied Microbiology and Biotechnology
  • Ecology

Cite this

Expanding the limits of thermoacidophily in the archaeon Sulfolobus solfataricus by adaptive evolution. / McCarthy, Samuel; Johnson, Tyler; Pavlik, Benjamin J.; Payne, Sophie; Schackwitz, Wendy; Martin, Joel; Lipzen, Anna; Keffeler, Erica; Blum, Paul H.

In: Applied and environmental microbiology, Vol. 82, No. 3, 01.01.2016, p. 857-867.

Research output: Contribution to journalArticle

McCarthy, S, Johnson, T, Pavlik, BJ, Payne, S, Schackwitz, W, Martin, J, Lipzen, A, Keffeler, E & Blum, PH 2016, 'Expanding the limits of thermoacidophily in the archaeon Sulfolobus solfataricus by adaptive evolution', Applied and environmental microbiology, vol. 82, no. 3, pp. 857-867. https://doi.org/10.1128/AEM.03225-15
McCarthy, Samuel ; Johnson, Tyler ; Pavlik, Benjamin J. ; Payne, Sophie ; Schackwitz, Wendy ; Martin, Joel ; Lipzen, Anna ; Keffeler, Erica ; Blum, Paul H. / Expanding the limits of thermoacidophily in the archaeon Sulfolobus solfataricus by adaptive evolution. In: Applied and environmental microbiology. 2016 ; Vol. 82, No. 3. pp. 857-867.
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