title: Molecular insight into bacterial cleavage of oceanic dimethylsulfoniopropionate into dimethyl sulfide.
abstract: The microbial cleavage of dimethylsulfoniopropionate (DMSP) generates volatile DMS through the action of DMSP lyases and is important in the global sulfur and carbon cycles. When released into the atmosphere from the oceans, DMS is oxidized, forming cloud condensation nuclei that may influence weather and climate. Six different DMSP lyase genes are found in taxonomically diverse microorganisms, and dddQ is among the most abundant in marine metagenomes. Here, we examine the molecular mechanism of DMSP cleavage by the DMSP lyase, DddQ, from Ruegeria lacuscaerulensis ITI_1157. The structures of DddQ bound to an inhibitory molecule 2-(N-morpholino)ethanesulfonic acid and of DddQ inactivated by a Tyr131Ala mutation and bound to DMSP were solved. DddQ adopts a β-barrel fold structure and contains a Zn(2+) ion and six highly conserved hydrophilic residues (Tyr120, His123, His125, Glu129, Tyr131, and His163) in the active site. Mutational and biochemical analyses indicate that these hydrophilic residues are essential to catalysis. In particular, Tyr131 undergoes a conformational change during catalysis, acting as a base to initiate the β-elimination reaction in DMSP lysis. Moreover, structural analyses and molecular dynamics simulations indicate that two loops over the substrate-binding pocket of DddQ can alternate between "open" and "closed" states, serving as a gate for DMSP entry. We also propose a molecular mechanism for DMS production through DMSP cleavage. Our study provides important insight into the mechanism involved in the conversion of DMSP into DMS, which should lead to a better understanding of this globally important biogeochemical reaction.
authors.affiliation: State Key Laboratory of Microbial Technology and Marine Biotechnology Research Center, Shandong University, Jinan 250100, China.
authors.forename: Chun-Yang
authors.initials: CY
authors.lastname: Li
authors.forename: Tian-Di
authors.initials: TD
authors.lastname: Wei
authors.forename: Sheng-Hui
authors.initials: SH
authors.lastname: Zhang
authors.forename: Xiu-Lan
authors.initials: XL
authors.lastname: Chen
authors.forename: Xiang
authors.initials: X
authors.lastname: Gao
authors.forename: Peng
authors.initials: P
authors.lastname: Wang
authors.forename: Bin-Bin
authors.initials: BB
authors.lastname: Xie
authors.forename: Hai-Nan
authors.initials: HN
authors.lastname: Su
authors.forename: Qi-Long
authors.initials: QL
authors.lastname: Qin
authors.forename: Xi-Ying
authors.initials: XY
authors.lastname: Zhang
authors.forename: Juan
authors.initials: J
authors.lastname: Yu
authors.forename: Hong-Hai
authors.initials: HH
authors.lastname: Zhang
authors.forename: Bai-Cheng
authors.initials: BC
authors.lastname: Zhou
authors.forename: Gui-Peng
authors.initials: GP
authors.lastname: Yang
authors.forename: Yu-Zhong
authors.initials: YZ
authors.lastname: Zhang
mesh_terms: D020561:Alphaproteobacteria / Q000378:metabolism*; D000595:Amino Acid Sequence; D002244:Carbon / Q000737:chemistry; D057486:Carbon Cycle; D013437:Carbon-Sulfur Lyases / Q000737:chemistry; D002384:Catalysis; D020134:Catalytic Domain; D002942:Circular Dichroism; D018360:Crystallography, X-Ray; D004252:DNA Mutational Analysis; D008670:Metals / Q000737:chemistry; D056004:Molecular Dynamics Simulation; D008969:Molecular Sequence Data; D009792:Oceans and Seas; D010100:Oxygen / Q000737:chemistry; D011485:Protein Binding; D017510:Protein Folding; D017433:Protein Structure, Secondary; D013440:Sulfides / Q000737:chemistry*; D013452:Sulfonium Compounds / Q000737:chemistry*; D013455:Sulfur / Q000737:chemistry; D014871:Water Microbiology; D015032:Zinc / Q000737:chemistry
chemical_list: D008670:Metals; D013440:Sulfides; D013452:Sulfonium Compounds; D013455:Sulfur; D002244:Carbon; C068078:dimethylpropiothetin; D013437:Carbon-Sulfur Lyases; C400924:dimethylsulfoniopropionate lyase; D015032:Zinc; C004784:dimethyl sulfide; D010100:Oxygen
keywords: DMS generation; DMSP cleavage mechanism; DMSP lyase DddQ; DMSP lyase structure; marine bacteria