Geobiological feedbacks and the evolution of thermoacidophiles

Daniel R. Colman, Saroj Poudel, Trinity L. Hamilton, Jeff R. Havig, Matthew J. Selensky, Everett Shock, Eric S. Boyd

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Oxygen-dependent microbial oxidation of sulfur compounds leads to the acidification of natural waters. How acidophiles and their acidic habitats evolved, however, is largely unknown. Using 16S rRNA gene abundance and composition data from 72 hot springs in Yellowstone National Park, Wyoming, we show that hyperacidic (pH<3.0) hydrothermal ecosystems are dominated by a limited number of archaeal lineages with an inferred ability to respire O 2. Phylogenomic analyses of 584 existing archaeal genomes revealed that hyperacidophiles evolved independently multiple times within the Archaea, each coincident with the emergence of the ability to respire O 2, and that these events likely occurred in the recent evolutionary past. Comparative genomic analyses indicated that archaeal thermoacidophiles from independent lineages are enriched in similar protein-coding genes, consistent with convergent evolution aided by horizontal gene transfer. Because the generation of acidic environments and their successful habitation characteristically require O 2, these results suggest that thermoacidophilic Archaea and the acidity of their habitats co-evolved after the evolution of oxygenic photosynthesis. Moreover, it is likely that dissolved O 2 concentrations in thermal waters likely did not reach levels capable of sustaining aerobic thermoacidophiles and their acidifying activity until ∼0.8 Ga, when present day atmospheric levels were reached, a time period that is supported by our estimation of divergence times for archaeal thermoacidophilic clades.

Original languageEnglish (US)
Pages (from-to)225-236
Number of pages12
JournalISME Journal
Volume12
Issue number1
DOIs
StatePublished - Jan 1 2018

Fingerprint

Archaea
Ecosystem
hot springs
convergent evolution
Archaeal Genome
habitats
Hot Springs
acidification
acidity
Sulfur Compounds
Horizontal Gene Transfer
national parks
sulfur
genes
thermal water
Water
gene
gene transfer
sulfur compound
Photosynthesis

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Colman, D. R., Poudel, S., Hamilton, T. L., Havig, J. R., Selensky, M. J., Shock, E., & Boyd, E. S. (2018). Geobiological feedbacks and the evolution of thermoacidophiles. ISME Journal, 12(1), 225-236. https://doi.org/10.1038/ismej.2017.162

Geobiological feedbacks and the evolution of thermoacidophiles. / Colman, Daniel R.; Poudel, Saroj; Hamilton, Trinity L.; Havig, Jeff R.; Selensky, Matthew J.; Shock, Everett; Boyd, Eric S.

In: ISME Journal, Vol. 12, No. 1, 01.01.2018, p. 225-236.

Research output: Contribution to journalArticle

Colman, DR, Poudel, S, Hamilton, TL, Havig, JR, Selensky, MJ, Shock, E & Boyd, ES 2018, 'Geobiological feedbacks and the evolution of thermoacidophiles', ISME Journal, vol. 12, no. 1, pp. 225-236. https://doi.org/10.1038/ismej.2017.162
Colman DR, Poudel S, Hamilton TL, Havig JR, Selensky MJ, Shock E et al. Geobiological feedbacks and the evolution of thermoacidophiles. ISME Journal. 2018 Jan 1;12(1):225-236. https://doi.org/10.1038/ismej.2017.162
Colman, Daniel R. ; Poudel, Saroj ; Hamilton, Trinity L. ; Havig, Jeff R. ; Selensky, Matthew J. ; Shock, Everett ; Boyd, Eric S. / Geobiological feedbacks and the evolution of thermoacidophiles. In: ISME Journal. 2018 ; Vol. 12, No. 1. pp. 225-236.
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