Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons

Baozhan Wang,Xue Zhou,Meng Li,Xin Yan,Yue Zheng,Yi Ren,Willm Martens‐Habbena ,Emiley A Eloe‐Fadrosh ,Ping Han,Michael Wagner,Wei Qin,Douglas H Bartlett,Yang Liu,Lu Lu,A E Ingalls ,Linmeng Liu,Man‐Young Jung ,Craig W Herbold,Cheryl Heiner,Junbin Ji,Richard J Hall ,David A Stahl,Li Huang,Sung‐Keun Rhee ,Zhongjun Jia

doi:10.1038/s41396-019-0493-x

Abstract

Thaumarchaeota are responsible for a significant fraction of ammonia oxidation in the oceans and in soils that range from alkaline to acidic. However, the adaptive mechanisms underpinning their habitat expansion remain poorly understood. Here we show that expansion into acidic soils and the high pressures of the hadopelagic zone of the oceans is tightly linked to the acquisition of a variant of the energy-yielding ATPases via horizontal transfer. Whereas the ATPase genealogy of neutrophilic Thaumarchaeota is congruent with their organismal genealogy inferred from concatenated conserved proteins, a common clade of V-type ATPases unites phylogenetically distinct clades of acidophilic/acid-tolerant and piezophilic/piezotolerant species. A presumptive function of pumping cytoplasmic protons at low pH is consistent with the experimentally observed increased expression of the V-ATPase in an acid-tolerant thaumarchaeote at low pH. Consistently, heterologous expression of the thaumarchaeotal V-ATPase significantly increased the growth rate of E. coli at low pH. Its adaptive significance to growth in ocean trenches may relate to pressure-related changes in membrane structure in which this complex molecular machine must function. Together, our findings reveal that the habitat expansion of Thaumarchaeota is tightly correlated with extensive horizontal transfer of atp operons.

Highlights

The ammonia-oxidizing archaea (AOA) are among the most abundant and ubiquitous microorganisms on Earth [1,2,3]
Following the initial description of Nitrosopumilus maritimus SCM1 [10, 11], analysis of the physiology of AOA has been aided by cultivation of additional ecotypes, including neutrophilic Nitrososphaera species and obligately acidophilic Candidatus (Ca.) Nitrosotalea devanaterra Nd1 isolated from soils [12,13,14], and thermophilic Nitrosocaldus species enriched from geothermal habitats [15,16,17]
Since AOA are united by a single autotrophic metabolism dependent on ATP generation via a proton motive force (PMF), we examined the possible role that variation in ATPase composition and structure might play in their adaptive radiation into environments of low pH and high pressure

Summary

Introduction

The ammonia-oxidizing archaea (AOA) are among the most abundant and ubiquitous microorganisms on Earth [1,2,3]. Since AOA are united by a single autotrophic metabolism dependent on ATP generation via a PMF, we examined the possible role that variation in ATPase composition and structure might play in their adaptive radiation into environments of low pH and high pressure. Stable isotope probing (SIP) with 13C-labeled CO2 was used to selectively recover DNA from metabolically active AOA in acidic soils, significantly expanding the genomic representation of Thaumarchaeota active in acidic environments through the assembly of two novel genomes. Comparative analysis of these and available archaeal genomes and genomic fragments was used to explore the evolutionary diversification of ATPases in relationship to archaeal habitats of varying pH and hydrostatic pressure. The functional significance of this variant to adaptation to low pH is supported by our observations showing (i) increased transcription of the ATPase variant genes by an acid-tolerant AOA following transition from neutral to acidic growth conditions and (ii) higher growth rates at low pH of an Escherichia coli (E. coli) genetically modified to express the archaeal variant

Materials and methods

Results and discussion

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