title: Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota.
abstract: The Thaumarchaeota is an abundant and ubiquitous phylum of archaea that plays a major role in the global nitrogen cycle. Previous analyses of the ammonia monooxygenase gene amoA suggest that pH is an important driver of niche specialization in these organisms. Although the ecological distribution and ecophysiology of extant Thaumarchaeota have been studied extensively, the evolutionary rise of these prokaryotes to ecological dominance in many habitats remains poorly understood. To characterize processes leading to their diversification, we investigated coevolutionary relationships between amoA, a conserved marker gene for Thaumarchaeota, and soil characteristics, by using deep sequencing and comprehensive environmental data in Bayesian comparative phylogenetics. These analyses reveal a large and rapid increase in diversification rates during early thaumarchaeotal evolution; this finding was verified by independent analyses of 16S rRNA. Our findings suggest that the entire Thaumarchaeota diversification regime was strikingly coupled to pH adaptation but less clearly correlated with several other tested environmental factors. Interestingly, the early radiation event coincided with a period of pH adaptation that enabled the terrestrial Thaumarchaeota ancestor to initially move from neutral to more acidic and alkaline conditions. In contrast to classic evolutionary models, whereby niches become rapidly filled after adaptive radiation, global diversification rates have remained stably high in Thaumarchaeota during the past 400-700 million years, suggesting an ongoing high rate of niche formation or switching for these microbes. Our study highlights the enduring importance of environmental adaptation during thaumarchaeotal evolution and, to our knowledge, is the first to link evolutionary diversification to environmental adaptation in a prokaryotic phylum.
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 2TZ, United Kingdom; c.rangin@abdn.ac.uk.
authors.forename: Cécile
authors.initials: C
authors.lastname: Gubry-Rangin
authors.affiliation: Department for Computational Biology of Infection Research, Helmholtz Center for Infection Research, 38124 Braunschweig, Germany;
authors.forename: Christina
authors.initials: C
authors.lastname: Kratsch
authors.affiliation: Institute for Cell and Molecular Biosciences, University of Newcastle, Newcastle, NE2 4HH, United Kingdom.
authors.forename: Tom A
authors.initials: TA
authors.lastname: Williams
authors.affiliation: Department for Computational Biology of Infection Research, Helmholtz Center for Infection Research, 38124 Braunschweig, Germany;
authors.forename: Alice C
authors.initials: AC
authors.lastname: McHardy
authors.affiliation: Institute for Cell and Molecular Biosciences, University of Newcastle, Newcastle, NE2 4HH, United Kingdom.
authors.forename: T Martin
authors.initials: TM
authors.lastname: Embley
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 2TZ, United Kingdom;
authors.forename: James I
authors.initials: JI
authors.lastname: Prosser
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 2TZ, United Kingdom;
authors.forename: Daniel J
authors.initials: DJ
authors.lastname: Macqueen
mesh_terms: D000641:Ammonia / Q000737:chemistry; D001105:Archaea / Q000201:enzymology / Q000235:genetics / Q000502:physiology*; D001499:Bayes Theorem; D005075:Biological Evolution; D016000:Cluster Analysis; D019143:Evolution, Molecular; D006863:Hydrogen-Ion Concentration; D008968:Molecular Conformation; D009584:Nitrogen / Q000737:chemistry; D010088:Oxidoreductases / Q000235:genetics* / Q000378:metabolism; D010100:Oxygen / Q000737:chemistry; D010802:Phylogeny; D012336:RNA, Ribosomal, 16S / Q000378:metabolism; D011994:Recombinant Proteins / Q000737:chemistry; D012987:Soil / Q000737:chemistry*
chemical_list: D012336:RNA, Ribosomal, 16S; D011994:Recombinant Proteins; D012987:Soil; D000641:Ammonia; D010088:Oxidoreductases; C045582:ammonia monooxygenase; D009584:Nitrogen; D010100:Oxygen
keywords: Thaumarchaeota; ammonia oxidation; archaea; diversification; phylogeny