Anaerobic oxidation of long-chain n-alkanes by the hyperthermophilic sulfate-reducing archaeon, Archaeoglobus fulgidus.
The thermophilic sulfate-reducing archaeon Archaeoglobus fulgidus strain VC-16 (DSM 4304), which is known to oxidize fatty acids and n-alkenes, was shown to oxidize saturated hydrocarbons (n-alkanes in the range C10-C21) with thiosulfate or sulfate as a terminal electron acceptor. The amount of n-hexadecane degradation observed was in stoichiometric agreement with the theoretically expected amount of thiosulfate reduction. One of the pathways used by anaerobic microorganisms to activate alkanes is addition to fumarate that involves alkylsuccinate synthase as a key enzyme. A search for genes encoding homologous enzymes in A. fulgidus identified the pflD gene (locus-tag AF1449) that was previously annotated as a pyruvate formate lyase. A phylogenetic analysis revealed that this gene is of bacterial origin and was likely acquired by A. fulgidus from a bacterial donor through a horizontal gene transfer. Based on three-dimensional modeling of the corresponding protein and molecular dynamic simulations, we hypothesize an alkylsuccinate synthase activity for this gene product. The pflD gene expression was upregulated during the growth of A. fulgidus on an n-alkane (C16) compared with growth on a fatty acid. Our results suggest that anaerobic alkane degradation in A. fulgidus may involve the gene pflD in alkane activation through addition to fumarate. These findings highlight the possible importance of hydrocarbon oxidation at high temperatures by A. fulgidus in hydrothermal vents and the deep biosphere.
Aix Marseille Université, CNRS, Université de Toulon, IRD, MIO UM 110, Marseille, France.
Nadia
N
Khelifi
Aix Marseille Université, CNRS, Université de Toulon, IRD, MIO UM 110, Marseille, France.
Oulfat
O
Amin Ali
Centre de Recherche en Cancérologie de Marseille (CRCM), CNRS UMR 7258, INSERM U 1068, Institut Paoli-Calmettes, Aix Marseille Université, Marseille, France.
Philippe
P
Roche
Université de Lyon, Université Lyon 1, CNRS, UMR 5276, Laboratoire de Géologie de Lyon, Villeurbanne, France.
Vincent
V
Grossi
Université de Lyon, Université Lyon 1, CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, Villeurbanne, France.
Céline
C
Brochier-Armanet
Aix Marseille Université, CNRS, LCB UMR 7283, Marseille, France.
Odile
O
Valette
Aix Marseille Université, CNRS, Université de Toulon, IRD, MIO UM 110, Marseille, France.
Bernard
B
Ollivier
Aix Marseille Université, CNRS, LCB UMR 7283, Marseille, France.
Alain
A
Dolla
Aix Marseille Université, CNRS, Université de Toulon, IRD, MIO UM 110, Marseille, France.
Agnès
A
Hirschler-Réa
D000473:Alkanes / Q000378:metabolism*; D000693:Anaerobiosis; D019843:Archaeal Proteins / Q000737:chemistry / Q000145:classification / Q000235:genetics / Q000378:metabolism; D019611:Archaeoglobus fulgidus / Q000201:enzymology / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D005227:Fatty Acids / Q000378:metabolism; D006358:Hot Temperature; D010084:Oxidation-Reduction; D010802:Phylogeny; D013431:Sulfates / Q000378:metabolism
D000473:Alkanes; D019843:Archaeal Proteins; D005227:Fatty Acids; D013431:Sulfates; C007932:n-hexadecane