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 nonconvergent 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.
Highlights
Molecular evolutionary analyses are widely used in ecology and evolution to understand the genetic diversity of organisms
Phylogenetic reconstruction of ammonia monooxygenase subunit A (amoA) thaumarchaeotal sequences representing extensive mesophilic terrestrial diversity and diverse pH conditions has been recently used to demonstrate that pH adaptation occurred during thaumarchaeotal evolution, leading to several pHadapted lineages (Gubry-Rangin et al 2011, 2015)
In a phylogenetic framework, we place a priori significance on the ancestral branches where pH adaptation first occurred and make the following predictions: (i) because ammonia monooxygenase subunit A (AmoA) function is essential for energy production, it is highly conserved and a predominant signal of purifying selection should exist across the thaumarchaeotal phylogeny, (ii) but despite this, AmoA underwent episodic periods of adaptation concurrent to major pH specialization events, and (iii) amino acid changes fixed along branches where pH adaptation first occurred and have subsequently remained invariant in pH-adapted lineages are strong candidates to represent substitutions of persistent adaptive value in pH-specialized lineages
Summary
Molecular evolutionary analyses are widely used in ecology and evolution to understand the genetic diversity of organisms. Among the widely distributed nonpathogenic prokaryotes, Thaumarchaeota have been highly studied over the last decade, owing largely to their key nitrification function (which is central to the global nitrogen cycle) and massive abundance in marine and terrestrial ecosystems This microbial phylum is phylogenetically diverse (Gubry-Rangin et al 2011, 2015; Pester et al 2012; Vico Oton et al 2015) and specialized to a number of environmental conditions (Hatzenpichler 2012). À12960.4 26250.5 À12832.3 26221.3 4.570‡ 16.4 À12840.5 26235.6
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