Marine planktonic predator-prey interactions occur in microscale seascapes, where diffusing chemicals may act either as chemotactic cues that enhance or arrest predation, or as elemental resources that are complementary to prey ingestion. The phytoplankton osmolyte dimethylsulfoniopropionate (DMSP) and its degradation products dimethylsulfide (DMS) and acrylate are pervasive compounds with high chemotactic potential, but there is a longstanding controversy over whether they act as grazing enhancers or deterrents. Here, we investigated the chemotactic responses of three herbivorous dinoflagellates to point-sourced, microscale gradients of dissolved DMSP, DMS, and acrylate. We found no evidence for acrylate being a chemotactic repellent and observed a weak attractor role of DMS. DMSP behaved as a strong chemoattractor whose potential for grazing facilitation through effects on swimming patterns and aggregation depends on the grazer\'s feeding mode and ability to incorporate DMSP. Our study reveals that predation models will fail to predict grazing impacts unless they incorporate chemotaxis-driven searching and finding of prey.

Dimethylsulfoniopropionate (DMSP) is an abundant marine organosulfur compound with roles in stress protection, chemotaxis, nutrient and sulfur cycling and climate regulation. Here we report the discovery of a bifunctional DMSP biosynthesis enzyme, DsyGD, in the transamination pathway of the rhizobacterium Gynuella sunshinyii and some filamentous cyanobacteria not previously known to produce DMSP. DsyGD produces DMSP through its N-terminal DsyG methylthiohydroxybutyrate S-methyltransferase and C-terminal DsyD dimethylsulfoniohydroxybutyrate decarboxylase domains. Phylogenetically distinct DsyG-like proteins, termed DSYE, with methylthiohydroxybutyrate S-methyltransferase activity were found in diverse and environmentally abundant algae, comprising a mix of low, high and previously unknown DMSP producers. Algae containing DSYE, particularly bloom-forming Pelagophyceae species, were globally more abundant DMSP producers than those with previously described DMSP synthesis genes. This work greatly increases the number and diversity of predicted DMSP-producing organisms and highlights the importance of Pelagophyceae and other DSYE-containing algae in global DMSP production and sulfur cycling.

A series of mono- and heteronuclear platinum(II) and zinc(II) complexes with 4,4\',4″-tri-tert-butyl-2,2\':6\',2″-terpyridine ligand were synthesized and characterized. The DNA and protein binding properties of [ZnCl2(terpytBu)] (C1), [{cis-PtCl(NH3)2(μ-pyrazine)ZnCl(terpytBu)}](ClO4)2 (C2), [{trans-PtCl(NH3)2(μ-pyrazine)ZnCl(terpytBu)}](ClO4)2 (C3), [{cis-PtCl(NH3)2(μ-4,4\'-bipyridyl)ZnCl(terpytBu)}](CIO4)2 (C4) and [{trans-PtCl(NH3)2(μ-4,4\'-bipyridyl)ZnCl(terpytBu)}](CIO4)2 (C5) (where terpytBu = 4,4\',4″-tri-tert-butyl-2,2\':6\',2″-terpyridine), were investigated by electronic absorption, fluorescence spectroscopic, and molecular docking methods. Complexes featuring transplatin exhibited lower Kb and Ksv constant values compared to cisplatin analogs. The lowest Ksv value belonged to complex C1, while C4 exhibited the highest. Molecular docking studies reveal that the binding of complex C1 to DNA is due to van der Waals forces, while that of C2-C5 is due to conventional hydrogen bonds and van der Waals forces. The tested complexes exhibited variable cytotoxicity toward mouse colorectal carcinoma (CT26), human colorectal carcinoma (HCT116 and SW480), and non-cancerous mouse mesenchymal stem cells (mMSC). Particularly, the mononuclear C1 complex showed pronounced selectivity toward cancer cells over non-cancerous mMSC. The C1 complex notably induced apoptosis in CT26 cells, effectively arrested the cell cycle in the G0/G1 phase, and selectively down-regulated Cyclin D.

Methanethiol (MT) is a sulfur-containing compound produced during dimethylsulfoniopropionate (DMSP) degradation by marine bacteria. The C-S bond of MT can be cleaved by methanethiol oxidases (MTOs) to release a sulfur atom. However, the cleaving process remains unclear, and the species of sulfur product is uncertain. It has long been assumed that MTOs produce hydrogen sulfide (H2S) from MT. Herein, we studied the MTOs in the Rhodobacteraceae family-whose members are important DMSP degraders ubiquitous in marine environments. We identified 57 MTOs from 1,904 Rhodobacteraceae genomes. These MTOs were grouped into two major clusters. Cluster 1 members share three conserved cysteine residues, while cluster 2 members contain one conserved cysteine residue. We examined the products of three representative MTOs both in vitro and in vivo. All of them produced sulfane sulfur other than H2S from MT. Their conserved cysteines are substrate-binding sites in which the MTO-S-S-CH3 complex is formed. This finding clarified the sulfur product of MTOs and enlightened the MTO-catalyzing process. Moreover, this study connected DMSP degradation with sulfane sulfur metabolism, filling a critical gap in the DMSP degradation pathway and representing new knowledge in the marine sulfur cycle field.
OBJECTIVE: This study overthrows a long-time assumption that methanethiol oxidases (MTOs) cleave the C-S bond of methanethiol to produce both H2S and H2O2-the former is a strong reductant and the latter is a strong oxidant. From a chemistry viewpoint, this reaction is difficult to happen. Investigations on three representative MTOs indicated that sulfane sulfur (S0) was the direct product, and no H2O2 was produced. Finally, the products of MTOs were corrected to be S0 and H2O. This finding connected dimethylsulfoniopropionate (DMSP) degradation with sulfane sulfur metabolism, filling a critical gap in the DMSP degradation pathway and representing new knowledge in the marine sulfur cycle field.

The ability of marine bacteria to direct their movement in response to chemical gradients influences inter-species interactions, nutrient turnover, and ecosystem productivity. While many bacteria are chemotactic towards small metabolites, marine organic matter is predominantly composed of large molecules and polymers. Yet, the signalling role of these large molecules is largely unknown. Using in situ and laboratory-based chemotaxis assays, we show that marine bacteria are strongly attracted to the abundant algal polysaccharides laminarin and alginate. Unexpectedly, these polysaccharides elicited stronger chemoattraction than their oligo- and monosaccharide constituents. Furthermore, chemotaxis towards laminarin was strongly enhanced by dimethylsulfoniopropionate (DMSP), another ubiquitous algal-derived metabolite. Our results indicate that DMSP acts as a methyl donor for marine bacteria, increasing their gradient detection capacity and facilitating their access to polysaccharide patches. We demonstrate that marine bacteria are capable of strong chemotaxis towards large soluble polysaccharides and uncover a new ecological role for DMSP in enhancing this attraction. These navigation behaviours may contribute to the rapid turnover of polymers in the ocean, with important consequences for marine carbon cycling.

Endozoicomonas are often predominant bacteria and prominently important in coral health. Their role in dimethylsulfoniopropionate (DMSP) degradation has been a subject of discussion for over a decade. A previous study found that Endozoicomonas degraded DMSP through the dddD pathway. This process releases dimethyl sulfide, which is vital for corals coping with thermal stress. However, little is known about the related gene regulation and metabolic abilities of DMSP metabolism in Endozoicomonadaceae. In this study, we isolated a novel Endozoicomonas DMSP degrader and observed a distinct DMSP metabolic trend in two phylogenetically close dddD-harboring Endozoicomonas species, confirmed genetically by comparative transcriptomic profiling and visualization of the change of DMSP stable isotopes in bacterial cells using nanoscale secondary ion spectrometry. Furthermore, we found that DMSP cleavage enzymes are ubiquitous in coral Endozoicomonas with a preference for having DddD lyase. We speculate that harboring DMSP degrading genes enables Endozoicomonas to successfully colonize various coral species across the globe.

OBJECTIVE: Catabolism of dimethylsulfoniopropionate (DMSP) by marine bacteria has important impacts on the global sulfur cycle and climate. However, whether and how members of most oligotrophic bacterial groups participate in DMSP metabolism in marine environments remains largely unknown. In this study, by characterizing culturable strains, we have revealed that bacteria of the SAR92 clade, an abundant oligotrophic group of Gammaproteobacteria in coastal seawater, can catabolize DMSP through the DMSP lyase DddD-mediated cleavage pathway and/or the DMSP demethylase DmdA-mediated demethylation pathway to produce climate-active gases dimethylsulfide and methanethiol. Additionally, we found that SAR92 clade bacteria capable of catabolizing DMSP are widely distributed in global oceans. These results indicate that SAR92 clade bacteria are potentially important DMSP degraders and sources of climate-active gases in marine environments that have been overlooked, contributing to a better understanding of the roles and mechanisms of the oligotrophic bacteria in oceanic DMSP degradation.

Saltmarshes are highly productive environments, exhibiting high abundances of organosulfur compounds. Dimethylsulfoniopropionate (DMSP) is produced in large quantities by algae, plants, and bacteria and is a potential precursor for dimethylsulfoxide (DMSO) and dimethylsulfide (DMS). DMSO serves as electron acceptor for anaerobic respiration leading to DMS formation, which is either emitted or can be degraded by methylotrophic prokaryotes. Major products of these reactions are trace gases with positive (CO2, CH4) or negative (DMS) radiative forcing with contrasting effects on the global climate. Here, we investigated organic sulfur cycling in saltmarsh sediments and followed DMSO reduction in anoxic batch experiments. Compared to previous measurements from marine waters, DMSO concentrations in the saltmarsh sediments were up to ~300 fold higher. In batch experiments, DMSO was reduced to DMS and subsequently consumed with concomitant CH4 production. Changes in prokaryotic communities and DMSO reductase gene counts indicated a dominance of organisms containing the Dms-type DMSO reductases (e.g., Desulfobulbales, Enterobacterales). In contrast, when sulfate reduction was inhibited by molybdate, Tor-type DMSO reductases (e.g., Rhodobacterales) increased. Vibrionales increased in relative abundance in both treatments, and metagenome assembled genomes (MAGs) affiliated to Vibrio had all genes encoding the subunits of DMSO reductases. Molar conversion ratios of <1.3 CH4 per added DMSO were accompanied by a predominance of the methylotrophic methanogens Methanosarcinales. Enrichment of mtsDH genes, encoding for DMS methyl transferases in metagenomes of batch incubations indicate their role in DMS-dependent methanogenesis. MAGs affiliated to Methanolobus carried the complete set of genes encoding for the enzymes in methylotrophic methanogenesis.

Dimethylsulfoniopropionate (DMSP) and related organic sulfur compounds play key roles in global sulfur cycling. Bacteria have been found to be important DMSP producers in seawater and surface sediments of the aphotic Mariana Trench (MT). However, detailed bacterial DMSP cycling in the Mariana Trench subseafloor remains largely unknown. Here, the bacterial DMSP-cycling potential in a Mariana Trench sediment core (7.5 m in length) obtained at a 10,816-m water depth was investigated using culture-dependent and -independent methods. The DMSP content fluctuated along the sediment depth and reached the highest concentration at 15 to 18 cm below the seafloor (cmbsf). dsyB was the dominant known DMSP synthetic gene, existing in 0.36 to 1.19% of the bacteria, and was identified in the metagenome-assembled genomes (MAGs) of previously unknown bacterial DMSP synthetic groups such as Acidimicrobiia, Phycisphaerae, and Hydrogenedentia. dddP, dmdA, and dddX were the major DMSP catabolic genes. The DMSP catabolic activities of DddP and DddX retrieved from Anaerolineales MAGs were confirmed by heterologous expression, indicating that such anaerobic bacteria might participate in DMSP catabolism. Moreover, genes involved in methanethiol (MeSH) production from methylmercaptopropionate (MMPA) and dimethyl sulfide (DMS), MeSH oxidation, and DMS production were highly abundant, suggesting active conversions between different organic sulfur compounds. Finally, most culturable DMSP synthetic and catabolic isolates possessed no known DMSP synthetic and catabolic genes, and actinomycetes could be important groups involved in both DMSP synthesis and catabolism in Mariana Trench sediment. This study extends the current understanding of DMSP cycling in Mariana Trench sediment and highlights the need to uncover novel DMSP metabolic genes/pathways in extreme environments. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is an abundant organosulfur molecule in the ocean and is the precursor for the climate-active volatile gas dimethyl sulfide. Previous studies focused mainly on bacterial DMSP cycling in seawater, coastal sediment, and surface trench sediment samples, but DMSP metabolism in the Mariana Trench (MT) subseafloor sediments remains unknown. Here, we describe the DMSP content and metabolic bacterial groups in the subseafloor of the MT sediment. We found that the tendency for vertical variation of the DMSP content in the MT was distinct from that of the continent shelf sediment. Although dsyB and dddP were the dominant DMSP synthetic and catabolic genes in the MT sediment, respectively, both metagenomic and culture methods revealed multiple previously unknown DMSP metabolic bacterial groups, especially anaerobic bacteria and actinomycetes. The active conversion of DMSP, DMS, and methanethiol may also occur in the MT sediments. These results provide novel insights for understanding DMSP cycling in the MT.

Although the use of airborne molecules as infochemicals is common in terrestrial plants, it has not been shown to occur in an ecologically relevant context in marine seaweeds. Like terrestrial plants, intertidal plants spend part of their lives emersed at low tide and release volatile organic compounds (VOCs) into the air when they are grazed or physiologically stressed. We hypothesized seaweeds could use airborne VOCs as infochemicals and respond to them by upregulating a keystone defensive metabolite, dimethylsulfoniopropionate (DMSP). We conducted laboratory and field experiments in which Ulva fenestrata was exposed to airborne dimethyl sulfide (DMS), a volatile antiherbivore and antioxidant metabolite released when the seaweed is grazed or physiologically stressed. In the laboratory, U. fenestrata exposed to DMS had 43-48% higher DMSP concentrations, relative to controls, 6-9 days after exposure. In the field, U. fenestrata 1 m downwind of DMS emitters had 19% higher DMSP concentrations than upwind seaweeds after 11 days. To our knowledge, this is the first demonstration of a marine plant using an airborne molecule released when damaged to elicit defensive responses. Our study suggests that the ability to detect airborne compounds has evolved multiple times or before the divergence of terrestrial plants and green algae.