Molecular adaptation of Ammonia Monooxygenase during independent pH specialization in Thaumarchaeota

Daniel J. Macqueen, Cécile Gubry-Rangin

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Abstract

Microbes are abundant in nature and often highly adapted to local conditions. While great progress has been made in understanding the ecological factors driving their distribution in complex environments, the underpinning molecular-evolutionary mechanisms are rarely dissected. Therefore, we scrutinized the coupling of environmental and molecular adaptation in Thaumarchaeota, an abundant archaeal phylum with a key role in ammonia oxidation. These microbes are adapted to a diverse spectrum of environmental conditions, with pH being a key factor shaping their contemporary distribution and evolutionary diversification. We integrated high-throughput sequencing data spanning a broad representation of ammonia-oxidizing terrestrial lineages with codon modelling analyses, testing the hypothesis that ammonia monooxygenase subunit A (AmoA) - a highly conserved membrane protein crucial for ammonia oxidation and classical marker in microbial ecology - underwent adaptation during specialization to extreme pH environments. While purifying selection has been an important factor limiting AmoA evolution, we identified episodic shifts in selective pressure at the base of two phylogenetically-distant lineages that independently adapted to acidic conditions and subsequently gained lasting ecological success. This involved non-convergent selective mechanisms (positive selection vs. selection acting on variants fixed during an episode of relaxed selection) leading to unique sets of amino acid substitutions that remained fixed across the radiation of both acidophilic lineages, highlighting persistent adaptive value in acidic environments. Our data demonstrates distinct trajectories of AmoA evolution despite convergent phenotypic adaptation, suggesting that microbial environmental specialization can be associated with diverse signals of molecular adaptation, even for marker genes employed routinely by microbial ecologists.

Original languageEnglish
Pages (from-to)1986-1999
Number of pages14
JournalMolecular Ecology
Volume25
Issue number9
Early online date31 Mar 2016
DOIs
Publication statusPublished - May 2016

Fingerprint

Ammonia
ammonia
oxidation
microorganisms
convergent evolution
microbial ecology
amino acid substitution
Amino Acid Substitution
ecologists
Ecology
codons
Codon
membrane proteins
trajectories
Membrane Proteins
Radiation
environmental factors
genetic markers
limiting factor
Genes

Keywords

  • Evolutionary ecology
  • Environmental adaptation
  • Microbial evolution
  • Natural selection
  • Ammonia oxidation
  • archaea

Cite this

Molecular adaptation of Ammonia Monooxygenase during independent pH specialization in Thaumarchaeota. / Macqueen, Daniel J.; Gubry-Rangin, Cécile.

In: Molecular Ecology, Vol. 25, No. 9, 05.2016, p. 1986-1999.

Research output: Contribution to journalArticle

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