Abby, Sophie S.

Significance The marine sedimentary subsurface is a vast and inhospitable ecosystem, often described as a place where microbes “race to their death,” as microbial cells are buried and available energy is severely diminished with increasing depth/age. By combining a variety of biogeochemical and molecular methods to describe the energetics and genetics of the bacteria specialized in anaerobic ammonium oxidation, we show that despite prolonged exposure to highly unfavorable conditions for tens of thousands of years, these bacteria exhibit remarkable net population growth when reaching their niche: the nitrate–ammonium transition zone. This common, yet understudied, geochemical transition zone represents an oasis in the sedimentary energetic desert, and the growth it supports is of major importance for the global nitrogen cycle.

AbstractAmmonia 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 cultivated thermophilic representative with a sequenced genome, which allows to search for adaptive strategies and for traits that shape the evolution of Thaumarchaeota.CandidatusNitrosocaldus cavascurensis has been cultivated 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 25h. Phylogenetic analyses based on ribosomal proteins place the organism as a sister group to all known mesophilic AOA. The 1.58 Mb genome ofCa.N. cavascurensis harbors an amoAXCB gene cluster encoding ammonia monooxygenase, 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 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.