Candidatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome.

Sophie S Abby,Melina Kerou,Michaela Stieglmeier,Kevin Pfeifer,Christa Schleper,Mart Krupovic,Claudia Rossel,Michael Melcher

doi:10.3389/fmicb.2018.00028

Abstract

Ammonia oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread in moderate environments but their occurrence and activity has also been demonstrated in hot springs. Here we present the first enrichment of a thermophilic representative with a sequenced genome, which facilitates the search for adaptive strategies and for traits that shape the evolution of Thaumarchaeota. Candidatus Nitrosocaldus cavascurensis has been enriched from a hot spring in Ischia, Italy. It grows optimally at 68°C under chemolithoautotrophic conditions on ammonia or urea converting ammonia stoichiometrically into nitrite with a generation time of approximately 23 h. Phylogenetic analyses based on ribosomal proteins place the organism as a sister group to all known mesophilic AOA. The 1.58 Mb genome of Ca. N. cavascurensis harbors an amoAXCB gene cluster encoding ammonia monooxygenase and genes for a 3-hydroxypropionate/4-hydroxybutyrate pathway for autotrophic carbon fixation, but also genes that indicate potential alternative energy metabolisms. Although a bona fide gene for nitrite reductase is missing, the organism is sensitive to NO-scavenging, underlining the potential importance of this compound for AOA metabolism. Ca. N. cavascurensis is distinct from all other AOA in its gene repertoire for replication, cell division and repair. Its genome has an impressive array of mobile genetic elements and other recently acquired gene sets, including conjugative systems, a provirus, transposons and cell appendages. Some of these elements indicate recent exchange with the environment, whereas others seem to have been domesticated and might convey crucial metabolic traits.

Highlights

Ammonia oxidizing archaea (AOA) collectively classified as Nitrososphaeria within the phylum Thaumarchaeota (Brochier-Armanet et al, 2008; Spang et al, 2010; Stieglmeier et al, 2014; Kerou et al, 2016a) represent the sole archaeal group that is globally distributed in oxic environments efficiently competing with aerobic bacteria
A single phylotype of AOA but no AOB or Nitrospira/commamox was identified in the enrichment via amplification and sequencing of amoA and 16S rRNA gene fragments and the presence of a single AOA phylotype was confirmed by metagenomic sequencing
In high throughput sequencing analyses using general prokaryotic primers to amplify the V2/V4 region of the 16S rRNA gene we identified phylotypes of the Deinococcus/Thermus group comprising up to 97% of the bacterial contaminating sequences and to minor extent sequences related to the Chloroflexi and Armatimonadetes

Summary

Introduction

Ammonia oxidizing archaea (AOA) collectively classified as Nitrososphaeria within the phylum Thaumarchaeota (Brochier-Armanet et al, 2008; Spang et al, 2010; Stieglmeier et al, 2014; Kerou et al, 2016a) represent the sole archaeal group that is globally distributed in oxic environments efficiently competing with aerobic bacteria Because of their large numbers in the Thermophilic Thaumarchaeon Cultivation and Genome ocean plankton, in marine sediments, in lakes and in soils, AOA are considered one of the most abundant groups of prokaryotes on this planet (Schleper et al, 2005; Prosser and Nicol, 2008; Erguder et al, 2009; Schleper and Nicol, 2010; Pester et al, 2011; Hatzenpichler, 2012; Stahl and de la Torre, 2012; Offre et al, 2013). Nitric oxide (NO) has been suggested to be involved in the process, because NO production and re-consumption have been observed (Martens-Habbena et al, 2015; Kozlowski et al, 2016b) and the NO scavenger PTIO was shown to inhibit AOA at very low concentrations (Yan et al, 2012; Shen et al, 2013; Martens-Habbena et al, 2015)

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