Enantioselective transformation of phytoplankton-derived dihydroxypropanesulfonate by marine bacteria.

Chirality, a fundamental property of matter, is often overlooked in the studies of marine organic matter cycles. Dihydroxypropanesulfonate (DHPS), a globally abundant organosulfur compound, serves as an ecologically important currency for nutrient and energy transfer from phytoplankton to bacteria in the ocean. However, the chirality of DHPS in nature and its transformation remain unclear. Here, we developed a novel approach using chiral phosphorus-reagent labeling to separate DHPS enantiomers. Our findings demonstrated that at least one enantiomer of DHPS is present in marine diatoms and coccolithophores, and that both enantiomers are widespread in marine environments. A novel chiral-selective DHPS catabolic pathway was identified in marine Roseobacteraceae strains, where HpsO and HpsP dehydrogenases at the gateway to DHPS catabolism act specifically on R-DHPS and S-DHPS, respectively. R-DHPS is also a substrate for the dehydrogenase HpsN. All three dehydrogenases generate stable hydrogen bonds between the chirality-center hydroxyls of DHPS and highly conserved residues, and HpsP also form coordinate-covalent bonds between the chirality-center hydroxyls and Zn2+, which determines the mechanistic basis of strict stereoselectivity. We further illustrated the role of enzymatic promiscuity in the evolution of DHPS metabolism in Roseobacteraceae and SAR11. This study provides the first evidence of chirality's involvement in phytoplankton-bacteria metabolic currencies, opening a new avenue for understanding the ocean organosulfur cycle.

Investigating organic sulfur in estuarine and offshore environments: A combined field and cultivation approach.

Estuarine-offshore sediments accumulate substantial particulate organic matter, containing organic sulfur as a key component. However, the distribution and sources of organic sulfur in such environments remain poorly understood. This study investigated organic sulfur in the Yangtze River Estuary and adjacent East China Sea. Dissolved organic sulfur varied from 0.65 to 1.99 µmol/L (molar S:C 0.006-0.018), while particulate organic sulfur ranged from 0.42 to 2.69 µmol/L (molar S:C 0.007-0.082). Sedimentary organic sulfur exhibited a similar molar S:C ratio (0.014-0.071) to particulate organic sulfur in bottom water, implying that particulate matter deposition is a potential source. Furthermore, sediments exposed to frequent hypoxia harbored significantly higher organic sulfur and S:C values compared to non-hypoxic areas. Laboratory incubation experiments revealed the underlying mechanism: sustained activity of sulfate-reducing bacteria in hypoxic sediments led to a substantial increase in sedimentary organic sulfur (from 15 to 53 µmol/g) within 600 days. This microbially driven sulfurization rendered over 90 % of the organic sulfur resistant to acid hydrolysis. Therefore, this study demonstrates that, alongside particle deposition, microbial sulfurization significantly contributes to organic sulfur enrichment and likely promotes organic matter preservation in estuarine-offshore sediments, particularly under hypoxic conditions. This finding advances our understanding of organic sulfur sources in these vital ecosystems.

The microbial carbon pump and climate change.

The ocean has been a regulator of climate change throughout the history of Earth. One key mechanism is the mediation of the carbon reservoir by refractory dissolved organic carbon (RDOC), which can either be stored in the water column for centuries or released back into the atmosphere as CO2 depending on the conditions. The RDOC is produced through a myriad of microbial metabolic and ecological processes known as the microbial carbon pump (MCP). Here, we review recent research advances in processes related to the MCP, including the distribution patterns and molecular composition of RDOC, links between the complexity of RDOC compounds and microbial diversity, MCP-driven carbon cycles across time and space, and responses of the MCP to a changing climate. We identify knowledge gaps and future research directions in the role of the MCP, particularly as a key component in integrated approaches combining the mechanisms of the biological and abiotic carbon pumps for ocean negative carbon emissions.

Discovery of a novel marine Bacteroidetes with a rich repertoire of carbohydrate-active enzymes.

Members of the phylum Bacteroidetes play a key role in the marine carbon cycle through their degradation of polysaccharides via carbohydrate-active enzymes (CAZymes) and polysaccharide utilization loci (PULs). The discovery of novel CAZymes and PULs is important for our understanding of the marine carbon cycle. In this study, we isolated and identified a potential new genus of the family Catalimonadaceae, in the phylum Bacteroidetes, from the southwest Indian Ocean. Strain TK19036, the type strain of the new genus, is predicted to encode CAZymes that are relatively abundant in marine Bacteroidetes genomes. Tunicatimonas pelagia NBRC 107804T, Porifericola rhodea NBRC 107748T and Catalinimonas niigatensis NBRC 109829T, which exhibit 16 S rRNA similarities exceeding 90% with strain TK19036, and belong to the same family, were selected as reference strains. These organisms possess a highly diverse repertoire of CAZymes and PULs, which may enable them to degrade a wide range of polysaccharides, especially pectin and alginate. In addition, some secretory CAZymes in strain TK19036 and its relatives were predicted to be transported by type IX secretion system (T9SS). Further, to the best of our knowledge, we propose the first reported "hybrid" PUL targeting alginates in T. pelagia NBRC 107804T. Our findings provide new insights into the polysaccharide degradation capacity of marine Bacteroidetes, and suggest that T9SS may play a more important role in this process than previously believed.

Niche differentiation of microbial community shapes vertical distribution of recalcitrant dissolved organic matter in deep-sea sediments.

Sedimentary organic matter provides carbon substrates and energy sources for microorganisms, which drive benthic biogeochemical processes and in turn modify the quantity and quality of dissolved organic matter (DOM). However, the molecular composition and distribution of DOM and its interactions with microbes in deep-sea sediments remain poorly understood. Here, molecular composition of DOM and its relationship with microbes were analyzed in samples collected from two sediment cores (∼40 cm below the sea floor), at depths of 1157 and 2253 m from the South China Sea. Results show that niche differentiation was observed on a fine scale in different sediment layers, with Proteobacteria and Nitrososphaeria dominating the shallow sediments (0-6 cm) and Chloroflexi and Bathyarchaeia prevailing in deeper sediments (6-40 cm), indicating correspondence of microbial community composition with both geographical isolation and the availability of organic matter. An intimate link between the DOM composition and microbial community further indicates that, microbial mineralization of fresh organic matter in the shallow layer potentially resulted in the accumulation of recalcitrant DOM (RDOM), while relatively low abundance of RDOM was linked to anaerobic microbial utilization in deeper sediment layers. In addition, higher RDOM abundance in the overlying water, as compared to that in the surface sediment, suggests that sediment might be a source of deep-sea RDOM. These results emphasize the close relation between the distribution of sediment DOM and different microbial community, laying a foundation for understanding the complex dynamics of RDOM in deep-sea sediment and water column.

Eco-engineering approaches for ocean negative carbon emission.

The goal of achieving carbon neutrality in the next 30-40 years is approaching worldwide consensus and requires coordinated efforts to combat the increasing threat of climate change. Two main sets of actions have been proposed to address this grand goal. One is to reduce anthropogenic CO2 emissions to the atmosphere, and the other is to increase carbon sinks or negative emissions, i.e., removing CO2 from the atmosphere. Here we advocate eco-engineering approaches for ocean negative carbon emission (ONCE), aiming to enhance carbon sinks in the marine environment. An international program is being established to promote coordinated efforts in developing ONCE-relevant strategies and methodologies, taking into consideration ecological/biogeochemical processes and mechanisms related to different forms of carbon (inorganic/organic, biotic/abiotic, particulate/dissolved) for sequestration. We focus on marine ecosystem-based approaches and pay special attention to mechanisms that require transformative research, including those elucidating interactions between the biological pump (BP), the microbial carbon pump (MCP), and microbially induced carbonate precipitation (MICP). Eutrophic estuaries, hypoxic and anoxic waters, coral reef ecosystems, as well as aquaculture areas are particularly considered in the context of efforts to increase their capacity as carbon sinks. ONCE approaches are thus expected to be beneficial for both carbon sequestration and alleviation of environmental stresses.

Metabolism of chiral sulfonate compound 2,3-dihydroxypropane-1-sulfonate (DHPS) by Roseobacter bacteria in marine environment.

The sulfonate compound 2,3-dihydroxypropane-1-sulfonate (DHPS) is one of the most abundant organic sulfur compounds in the biosphere. DHPS derived from dietary intake could be transformed into sulfide by intestinal microbiota and thus impacts human health. However, little is known about its sulfur transformation and subsequent impacts in marine environment. In this study, laboratory-culturing was combined with targeted metabolomic, chemical fluorescence probing, and comparative proteomic methods to examine the bioavailability of chiral DHPS (R and S isomers) for bacteria belonging to the marine Roseobacter clade. The metabolic potential of DHPS in bacteria was further assessed based on genomic analysis. Roseobacter members Ruegeria pomeroyi DSS-3, Dinoroseobacter shibae DFL 12, and Roseobacter denitrificans OCh 114 could utilize chiral DHPS for growth, producing sulfite. They all contained a similar gene cluster for DHPS metabolism but differed in the genes encoding enzymes for desulfonation. There was no significant difference in the growth rate and DHPS consumption rate for R. pomeroyi DSS-3 between R- and S-DHPS cultures, with few proteins expressed differentially were found. Proteomic data suggested that a series of hydrogenases oxidized DHPS, after which desulfonation could proceed via three distinct enzymatic pathways. Strain R. pomeroyi DSS-3 completed the desulfonation via L-cysteate sulfo-lyase, while D. shibae DFL 12 and R. denitrificans OCh 114 primarily utilized sulfolactate sulfo-lyase, and sulfopyruvate decarboxylase followed by sulfoacetaldehyde acetyltransferase, respectively, to complete desulfonation releasing the sulfonate-moiety. The sulfite could be further oxidized or incorporated into sulfate assimilation, indicated by the proteomic data. Furthermore, DHPS metabolic pathways were found primarily in marine bacterial groups, including the majority of sequenced Roseobacter genomes. Our results suggest that chiral DHPS, as a vital reduced sulfur reservoir, could be metabolized by marine bacteria, providing a resource for bacterial growth, rather than acting as a source of toxic sulfide within the marine ecosystem.

Effects of environmental factors on denitrifying bacteria and functional genes in sediments of Bohai Sea, China.

The ability of denitrifying microorganisms to respond to different ecological pressures remains unknown, especially in marine sediments rich in various heavy metals. Here, gene abundance and transcriptional abundance of five functional denitrification genes (narG, nirK, nirS, norB, and nosZ) in Bohai Sea sediments were examined, and high-throughput Illumina sequencing was used to analyze the community structure of nirK and nirS denitrifying bacteria. The nirS- and nirK-type denitrifying bacteria were classified into different genera. The heavy metal content in sediments was negatively correlated with transcriptional abundance of denitrifying genes, and RNA: DNA ratio for each gene was highest in central Bohai Sea. These results indicated the distribution of nitrite reductase denitrifying bacterial communities was affected by depth, total nitrogen, total phosphorus and sediment grain size. Heavy metal contamination in sediment environment may negatively regulate the transcriptional abundance of denitrifying genes and cause geographical differences in the denitrifying bacterial community structure.