Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea)

• Published in: The ISME Journal Vol. 5; no. 6; pp. 945 - 961
• Main Authors: Yakimov, Michail M, Cono, Violetta La, Smedile, Francesco, DeLuca, Thomas H, Juárez, Silvia, Ciordia, Sergio, Fernández, Marisol, Albar, Juan Pablo, Ferrer, Manuel, Golyshin, Peter N, Giuliano, Laura
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.06.2011; Oxford University Press; Nature Publishing Group
• Subjects: 631/158/2446/2447; 631/158/853; 631/326/26; 631/337/475; Ammonia; Ammonia - metabolism; Autotrophic Processes; Biomedical and Life Sciences; Carbon - metabolism; Carbon dioxide fixation; Crenarchaeota - classification; Crenarchaeota - enzymology; Crenarchaeota - genetics; Crenarchaeota - metabolism; Deep sea; Ecology; Evolutionary Biology; Hydro-Lyases - genetics; Life Sciences; Marine ecosystems; Mediterranean Sea; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microorganisms; Molecular Sequence Data; Nitrogen; Nitrogen - metabolism; Original; original-article; Oxidation-Reduction; Oxidoreductases - genetics; Oxidoreductases - metabolism; Phylogeny; Physiology; Primary production; Proteins; RNA, Messenger - genetics; Seawater - chemistry; Seawater - microbiology; Urease - genetics; Urease - metabolism; Vertical distribution; Mediterranean Sea; A; crenarchaeal; C genes; Tyrrhenian Sea; K; dark ocean primary production; autotrophic; shotgun proteomics
• ISSN: 1751-7362; 1751-7370; 1751-7370
• DOI: 10.1038/ismej.2010.197

Mesophilic Crenarchaeota have recently been thought to be significant contributors to nitrogen (N) and carbon (C) cycling. In this study, we examined the vertical distribution of ammonia-oxidizing Crenarchaeota at offshore site in Southern Tyrrhenian Sea. The median value of the crenachaeal cell to amoA gene ratio was close to one suggesting that virtually all deep-sea Crenarchaeota possess the capacity to oxidize ammonia. Crenarchaea-specific genes, nir K and ure C, for nitrite reductase and urease were identified and their affiliation demonstrated the presence of ‘deep-sea’ clades distinct from ‘shallow’ representatives. Measured deep-sea dark CO 2 fixation estimates were comparable to the median value of photosynthetic biomass production calculated for this area of Tyrrhenian Sea, pointing to the significance of this process in the C cycle of aphotic marine ecosystems. To elucidate the pivotal organisms in this process, we targeted known marine crenarchaeal autotrophy-related genes, coding for acetyl-CoA carboxylase ( acc A) and 4-hydroxybutyryl-CoA dehydratase (4- hbd ). As in case of nir K and ure C, these genes are grouped with deep-sea sequences being distantly related to those retrieved from the epipelagic zone. To pair the molecular data with specific functional attributes we performed [ 14 C]HCO 3 incorporation experiments followed by analyses of radiolabeled proteins using shotgun proteomics approach. More than 100 oligopeptides were attributed to 40 marine crenarchaeal-specific proteins that are involved in 10 different metabolic processes, including autotrophy. Obtained results provided a clear proof of chemolithoautotrophic physiology of bathypelagic crenarchaeota and indicated that this numerically predominant group of microorganisms facilitate a hitherto unrecognized sink for inorganic C of a global importance.