Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota

Cecile Gubry-Rangin, Christina Kratsch, Tom A. Williams, Alice C. McHardy, T. Martin Embley, James I. Prosser, Daniel J. MacQueen

Research output: Contribution to journalArticle

33 Citations (Scopus)
4 Downloads (Pure)

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.
Original languageEnglish
Pages (from-to)9370-9375
Number of pages6
JournalPNAS
Volume112
Issue number30
Early online date13 Jul 2015
DOIs
Publication statusPublished - 28 Jul 2015

Fingerprint

niche
ecophysiology
adaptive radiation
nitrogen cycle
gene
prokaryote
ancestry
environmental factor
ammonia
phylogenetics
habitat
rate
soil
distribution
environmental data
organism
marker
radiation

Keywords

  • archaea
  • thaumarchaeota
  • pH
  • ammonia oxidation
  • evolution
  • diversification
  • phylogeny

Cite this

Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota. / Gubry-Rangin, Cecile; Kratsch, Christina ; Williams, Tom A. ; McHardy, Alice C. ; Embley, T. Martin; Prosser, James I.; MacQueen, Daniel J.

In: PNAS, Vol. 112, No. 30, 28.07.2015, p. 9370-9375.

Research output: Contribution to journalArticle

Gubry-Rangin, C, Kratsch, C, Williams, TA, McHardy, AC, Embley, TM, Prosser, JI & MacQueen, DJ 2015, 'Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota', PNAS, vol. 112, no. 30, pp. 9370-9375. https://doi.org/10.1073/pnas.1419329112
Gubry-Rangin, Cecile ; Kratsch, Christina ; Williams, Tom A. ; McHardy, Alice C. ; Embley, T. Martin ; Prosser, James I. ; MacQueen, Daniel J. / Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota. In: PNAS. 2015 ; Vol. 112, No. 30. pp. 9370-9375.
@article{04183d6d87034cff959b2ee295704f52,
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.",
keywords = "archaea, thaumarchaeota, pH, ammonia oxidation, evolution, diversification, phylogeny",
author = "Cecile Gubry-Rangin and Christina Kratsch and Williams, {Tom A.} and McHardy, {Alice C.} and Embley, {T. Martin} and Prosser, {James I.} and MacQueen, {Daniel J.}",
note = "This work was funded by a NERC fellowship (NE/J019151/1) to C.G.- R. T.M.E and T.A.W were supported by a European Research Grant ERC2010-AdG-268701. The authors also wish to thank Dr Anthony Travis (University of Aberdeen) for help with Bio-Linux.",
year = "2015",
month = "7",
day = "28",
doi = "10.1073/pnas.1419329112",
language = "English",
volume = "112",
pages = "9370--9375",
journal = "PNAS",
issn = "0027-8424",
publisher = "NATL ACAD SCIENCES",
number = "30",

}

TY - JOUR

T1 - Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota

AU - Gubry-Rangin, Cecile

AU - Kratsch, Christina

AU - Williams, Tom A.

AU - McHardy, Alice C.

AU - Embley, T. Martin

AU - Prosser, James I.

AU - MacQueen, Daniel J.

N1 - This work was funded by a NERC fellowship (NE/J019151/1) to C.G.- R. T.M.E and T.A.W were supported by a European Research Grant ERC2010-AdG-268701. The authors also wish to thank Dr Anthony Travis (University of Aberdeen) for help with Bio-Linux.

PY - 2015/7/28

Y1 - 2015/7/28

N2 - 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.

AB - 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.

KW - archaea

KW - thaumarchaeota

KW - pH

KW - ammonia oxidation

KW - evolution

KW - diversification

KW - phylogeny

U2 - 10.1073/pnas.1419329112

DO - 10.1073/pnas.1419329112

M3 - Article

VL - 112

SP - 9370

EP - 9375

JO - PNAS

JF - PNAS

SN - 0027-8424

IS - 30

ER -