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PMID: 21209665 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

The ISME journal ·Vol. 5 ·No. 6 ·2011-06-00 ·Pages 945-61

Yakimov MM, Cono VL, Smedile F, DeLuca TH, Juárez S, Ciordia S, Fernández M, Albar JP, Ferrer M, Golyshin PN, Giuliano L

Abstract

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, nirK and ureC, 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 (accA) and 4-hydroxybutyryl-CoA dehydratase (4-hbd). As in case of nirK and ureC, 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.

MeSH Terms
Ammonia/metabolism Autotrophic Processes Carbon/metabolism Crenarchaeota/classification,enzymology,genetics,metabolism Hydro-Lyases/genetics Mediterranean Sea Molecular Sequence Data Nitrogen/metabolism Oxidation-Reduction Oxidoreductases/genetics,metabolism Phylogeny RNA, Messenger/genetics Seawater/chemistry,microbiology Urease/genetics,metabolism
Chemicals
RNA, Messenger Carbon Ammonia Oxidoreductases nitric-oxide reductase ammonia monooxygenase Urease 4-hydroxybutyryl-CoA dehydratase Hydro-Lyases Nitrogen
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Yakimov Michail M
Laboratory of Marine Molecular Microbiology, Institute for Coastal Marine Environment, CNR, Messina, Italy. [email protected]
Cono Violetta La
Smedile Francesco
DeLuca Thomas H
Juárez Silvia
Ciordia Sergio
Fernández Marisol
Albar Juan Pablo
Ferrer Manuel
Golyshin Peter N
Giuliano Laura
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Article Info
Journal
The ISME journal
Abbr.
ISME J
ISSN
1751-7370
DOI
10.1038/ismej.2010.197
Email
[email protected]
Published
2011-06-00
Epub
2011-00-06
Pages
945-61
Language
English
Region
England
NLM ID
101301086
PMCID
PMC3131861
Subset
IM
Databases
GENBANK
HM241829, HM241830, HM241831, HM241832, HM241833, HM241834, HM241835, HM355483, HM355484, HM355485, HM355486, HM355487, HM355488, HM355489, HM355490, HM355491, HM355492, HM355493, HM355494, HM355495, HM355496, HM355497, HM355498, HM355499, HM355500, HM355501, HM355502, HM355503, HM355504, HM355505, HM355506, HM355507, HM355508, HM355509, HM355510, HM355511, HM355512, HM355513, HM355514, HM355515, HM355516, HM355517, HM355518, HM355519, HM355520, HM355521, HM355522, HM355523, HM355524, HM355525, HM355526, HM355527, HM355528, HM355529, HM355530, HM355531, HM355532, HM369442, HM369443, HM369444, HM369445, HM369446, HM369447, HM369448, HM369449, HM369450, HM369451, HM369452, HM369453, HM369454, HM369455, HM369456, HM369457, HQ339937, HQ339938, HQ339939, HQ339940, HQ339941, HQ339942, HQ339943, HQ339944, HQ339945, HQ339946, HQ339947, HQ339948, HQ339949, HQ339950, HQ339951
External Links
PubMed source DOI: 10.1038/ismej.2010.197 PMC Full Text View journal details
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