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

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.

Depth distributions of nitrite reductase (nirK) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay

“…Putative nirK genes were found in all but three of the screened AOA isolate/enrichment genomes, corroborating the postulated pivotal role of this gene in the core metabolism of mesophilic Thaumarchaeota. Exceptions were the uncultivated sponge symbiont Cenarchaeum symbiosum (Hallam et al, 2006b;Bartossek et al, 2010) and genomically characterized members of the thermophilic lineage Nitrosocaldus (Abby et al, 2018;Daebeler et al, 2018). Interestingly, some members of the mesophilic thaumarchaeal lineage -Nitrosopumilus maritimus SCM1 and Ca.…”

“…Nitrosocaldus cavascerensis and Ca. Nitrosocaldus islandicus (Abby et al, 2018;Daebeler et al, 2018).…”

Integrated mobile genetic elements in Thaumarchaeota

“…viennensis EN76 (Krupovic et al, 2011) and Ca. Nitrosocaldus cavascurensis SCU2 (Abby et al, 2018), respectively. The three new hits were in the genomes of Ca.…”

“…However, in the GenBank database it is affiliated to the phylum Thaumarchaeota and was, thus, retained in our analysis. The analysed organisms were isolated from a wide range of environments, including a subsurface gold mine (Nunoura et al, 2011), thermal springs (Spang et al, 2012;Lebedeva et al, 2013;Abby et al, 2018;Daebeler et al, 2018), wastewater treatment plant (Li et al, 2016), marine waters (Santoro et al, 2015;Bayer et al, 2016;Ahlgren et al, 2017) and sediments (Park et al, 2014) and various soil samples (Kim et al, 2011;Lehtovirta-Morley et al, 2011;Tourna et al, 2011;Zhalnina et al, 2014;Lehtovirta-Morley et al, 2016;Herbold et al, 2017). Although most of these organisms are mesophiles, some are psychrophilic (Hallam et al, 2006), thermophilic (Nunoura et al, 2011;Spang et al, 2012;Lebedeva et al, 2013;Abby et al, 2018;Daebeler et al, 2018) or acidophilic (Lehtovirta-Morley et al, 2011).…”

Bacterial Diversity in Feces of Wild Bald Eagles, Turkey Vultures and Common Ravens from the Pacific Northwest Coast, U.S.A

“…They have been found in the digestive tracts of some animals where they produce methane [48]; the role these organisms play in the gut of birds is still unknown [1]. Candidatus nitrosocaldus is ubiquitous in water environments being present in plankton, sediments, and surrounding soils of lakes and oceans [49]. It has a particular affinity for hot spring environments.…”