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.
370_sequence amoA tree: Bayesian amoA phylogenetic tree derived from 454 sequencing
Nucleotide alignment for the 370-sequence amoA tree: Nucleotide alignment (codon positions 1 and 2) for the 370-sequence amoA tree
508-sequence 16S rRNA tree: Bayesian 508-sequence phylogenetic 16S rRNA tree derived from merging non-redundant sequences available from the Silva database with non-redundant 454 dataset.
613_sequence amoA tree: Bayesian 613-sequence phylogenetic amoA tree derived from merging non-redundant sequences available from GenBank database with non-redundant 454 dataset.
Nucleotide alignment for the 508-sequence 16S rRNA tree: Nucleotide alignment for the 508-sequence 16S rRNA tree, derived from merging non-redundant sequences available from the Silva database with non-redundant 454 dataset.
Nucleotide alignment for the 613-sequence amoA tree: Nucleotide alignment for the 613-sequence amoA tree (codon positions 1 and 2), derived from merging non-redundant sequences available from GenBank database with non-redundant 454 dataset.
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- ammonia oxidation