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.

Controls of nitrogen cycling evaluated along a well‐characterized climate gradient

“…This is a critical process within the terrestrial nitrogen cycle, and may explain the positive relationship between archaeal diversity and nitrogen mineralization observed. Previous studies have found that the abundance of AOA is controlled by pH (Gubry-Rangin et al 2011, Gubry-Rangin et al 2015 and C:N ratio (Bates et al 2011), both of which influenced archaeal richness in our study as well. For Bacteria, richness was most consistently positively affected by pH (Table S1), consistent with other studies Jackson 2006, Lauber et al 2009).…”

Molecular adaptation of ammonia monooxygenase during independent pH specialization in Thaumarchaeota

“…) and a resultant set of 370 sequences, broadly representative of phylum‐scale diversity, was used to perform a joint Bayesian phylogenetic and relaxed molecular clock analysis after exclusion of confounding effects linked to recombination and mutational saturation (Gubry‐Rangin et al . ). An associated 370‐sequence in‐frame alignment representing 89% of the amoA coding sequence (missing 8 and 14 codons from the respective 5′ and 3′ of the alignment) was used for evolutionary analyses, along with an associated phylogenetic tree employed in evolutionary analyses.…”

“…Sampling of thaumarchaeotal a moA sequences and generation of phylogenetic trees used in this study have been described elsewhere (Gubry‐Rangin et al . , ). Briefly, high‐throughput sequencing was performed on 47 UK soils targeting the archaeal amoA gene (Gubry‐Rangin et al .…”

“…Interestingly, a strong link between pH and thaumarchaeotal diversity extends across vast evolutionary time, as reconstructed rates of pH adaptation and lineage diversification are tightly coupled over the phylum's entire evolutionary history – stretching over half a billion years (Gubry‐Rangin et al . ).…”

“…This microbial phylum is phylogenetically diverse (Gubry‐Rangin et al . , ; Pester et al . ; Vico Oton et al .…”