Nitrification, the oxidation of ammonia via nitrite to nitrate, has
always been considered as a two-step process catalyzed by chemolithoautotrophic
microorganisms oxidizing either ammonia or nitrite. No known nitrifier carries
out both steps, although complete nitrification should be energetically
advantageous. This functional separation has puzzled microbiologists for a
century. Here we report on the discovery and cultivation of a completely
nitrifying bacterium from the genus Nitrospira, a globally
distributed group of nitrite oxidizers. The genome of this chemolithoautotrophic
organism encodes both the pathways for ammonia and nitrite oxidation, which are
concomitantly expressed during growth by ammonia oxidation to nitrate. Genes
affiliated with the phylogenetically distinct ammonia monooxygenase and
hydroxylamine dehydrogenase genes of Nitrospira are present in
many environments and were retrieved on Nitrospira-contigs in
new metagenomes from engineered systems. These findings fundamentally change our
picture of nitrification and point to completely nitrifying
Nitrospira as key components of nitrogen-cycling microbial
communities.
Summary paragraphNitrification, the oxidation of ammonia (NH3) via nitrite
(NO2-) to nitrate (NO3-), is a
key process of the biogeochemical nitrogen cycle. For decades, ammonia and
nitrite oxidation were thought to be separately catalyzed by ammonia-oxidizing
bacteria (AOB) and archaea (AOA), and by nitrite-oxidizing bacteria (NOB). The
recent discovery of complete ammonia oxidizers (comammox) in the NOB genus
Nitrospira1,2, which alone convert ammonia to nitrate,
raised questions about the ecological niches where comammox
Nitrospira successfully compete with canonical nitrifiers.
Here we isolated the first pure culture of a comammox bacterium,
Nitrospira inopinata, and show that it is adapted to slow
growth in oligotrophic and dynamic habitats based on a high affinity for
ammonia, low maximum rate of ammonia oxidation, high growth yield compared to
canonical nitrifiers, and genomic potential for alternative metabolisms. The
nitrification kinetics of four AOA from soil and hot springs were determined for
comparison. Their surprisingly poor substrate affinities and lower growth yields
reveal that, in contrast to earlier assumptions, not all AOA are most
competitive in strongly oligotrophic environments and that N.
inopinata has the highest substrate affinity of all analyzed
ammonia oxidizer isolates except the marine AOA Nitrosopumilus
maritimus SCM13. These
results suggest a role of comammox organisms for nitrification under
oligotrophic and dynamic conditions.
The discovery of ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota and the high abundance of archaeal ammonia monooxygenase subunit A encoding gene sequences in many environments have extended our perception of nitrifying microbial communities. Moreover, AOA are the only aerobic ammonia oxidizers known to be active in geothermal environments. Molecular data indicate that in many globally distributed terrestrial high-temperature habits a thaumarchaeotal lineage within the Nitrosopumilus cluster (also called “marine” group I.1a) thrives, but these microbes have neither been isolated from these systems nor functionally characterized in situ yet. In this study, we report on the enrichment and genomic characterization of a representative of this lineage from a thermal spring in Kamchatka. This thaumarchaeote, provisionally classified as “Candidatus Nitrosotenuis uzonensis”, is a moderately thermophilic, non-halophilic, chemolithoautotrophic ammonia oxidizer. The nearly complete genome sequence (assembled into a single scaffold) of this AOA confirmed the presence of the typical thaumarchaeotal pathways for ammonia oxidation and carbon fixation, and indicated its ability to produce coenzyme F420 and to chemotactically react to its environment. Interestingly, like members of the genus Nitrosoarchaeum, “Candidatus N. uzonensis” also possesses a putative artubulin-encoding gene. Genome comparisons to related AOA with available genome sequences confirmed that the newly cultured AOA has an average nucleotide identity far below the species threshold and revealed a substantial degree of genomic plasticity with unique genomic regions in “Ca. N. uzonensis”, which potentially include genetic determinants of ecological niche differentiation.
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