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 substratebinding 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.DMSP lyase DddQ | DMSP lyase structure | DMS generation | DMSP cleavage mechanism | marine bacteria T he compatible solute dimethylsulfoniopropionate (DMSP) is produced worldwide in a large amount, ∼10 9 tons per annum, mainly by marine phytoplankton and macroalgae; thus, this compound is a major participant in the global sulfur and carbon cycles (1, 2). Some DMSP is broken down by the algae producing it (3), but it is primarily catabolized by marine bacteria via two pathways, the demethylation pathway and the cleavage pathway (4). In the demethylation pathway, DMSP is demethylated and the methylmercaptopropionate generated is subsequently demethiolated to release methanthiol, providing the marine microbial food web a source of reduced sulfur (4). In the cleavage pathway, DMSP is cleaved by DMSP lyases to generate DMS, an environmentally important gas, and acrylate (or 3-hydroxypropionate) (5). DMS is the major form of biogenic sulfur that enters the atmosphere from the oceans (6). Some 300 Tg of DMS is annually produced by microbial activities, about 10% of which is transferred from oceans to the atmosphere (7,8). DMS in the atmosphere can be photochemically oxidized into DMSO or sulfate aerosols (9), which can scatter solar radiation directly and also form cloud condensation nuclei that influence the reflectivity of clouds and thereby global temperature (9, 10). These s...

SummaryThe microbial cleavage of dimethylsulfoniopropionate (DMSP) generates volatile dimethyl sulfide (DMS) and is an important step in global sulfur and carbon cycles. DddP is a DMSP lyase in marine bacteria, and the deduced dddP gene product is abundant in marine metagenomic data sets. However, DddP belongs to the M24 peptidase family according to sequence alignment. Peptidases hydrolyze C-N bonds, but DddP is deduced to cleave C-S bonds. Mechanisms responsible for this striking functional shift are currently unknown. We determined the structures of DMSP lyase RlDddP (the DddP from Ruegeria lacuscaerulensis ITI_1157) bound to inhibitory 2-(N-morpholino) ethanesulfonic acid or PO 4 3− and of two mutants of RlDddP bound to acrylate. Based on structural, mutational and biochemical analyses, we characterized a new ion-shift catalytic mechanism of RlDddP for DMSP cleavage. Furthermore, we suggested the structural mechanism leading to the loss of peptidase activity and the subsequent development of DMSP lyase activity in DddP. This study sheds light on the catalytic mechanism and the divergent evolution of DddP, leading to a better understanding of marine bacterial DMSP catabolism and global DMS production.

Cryptophyte plastids originated from a red algal ancestor through secondary endosymbiosis. Cryptophyte photosystem I (PSI) associates with transmembrane alloxanthin-chlorophyll a/c proteins (ACPIs) as light-harvesting complexes (LHCs). Here we report the structure of the photosynthetic PSI–ACPI supercomplex from the cryptophyte Chroomonas placoidea at 2.7-Å resolution obtained by cryo-electron microscopy. Cryptophyte PSI–ACPI represents a unique PSI–LHCI intermediate in the evolution from red algal to diatom PSI–LHCI. The PSI–ACPI supercomplex is composed of a monomeric PSI core containing 14 subunits, 12 of which originated in red algae, one diatom PsaR homolog, and an additional peptide. The PSI core is surrounded by 14 ACPI subunits that form two antenna layers: an inner layer with 11 ACPIs surrounding the PSI core, and an outer layer containing 3 ACPIs. A pigment-binding subunit that is not present in any other previously characterized PSI–LHCI complexes, ACPI-S, mediates the association and energy transfer between the outer and inner ACPIs. The extensive pigment network of PSI–ACPI ensures efficient light harvesting, energy transfer, and dissipation. Overall, the PSI–LHCI structure identified in this study provides a framework for delineating the mechanisms of energy transfer in cryptophyte PSI–LHCI and for understanding the evolution of photosynthesis in the red lineage, which occurred via secondary endosymbiosis.