Biogenic production of DMSP and its degradation to DMS—their roles in the global sulfur cycle

Dimethyl sulfide(DMS) is the most abundant form of volatile sulfur in Earth's oceans, and is mainly produced by the enzymatic clevage of dimethylsulfoniopropionate(DMSP). DMS and DMSP play important roles in driving the global sulfur cycle and may affect climate. DMSP is proposed to serve as an osmolyte, a grazing deterrent, a signaling molecule, an antioxidant, a cryoprotectant and/or as a sink for excess sulfur. It was long believed that only marine eukaryotes such as phytoplankton produce DMSP. However, we recently discovered that marine heterotrophic bacteria can also produce DMSP, making them a potentially important source of DMSP. At present, one prokaryotic and two eukaryotic DMSP synthesis enzymes have been identified.Marine heterotrophic bacteria are likely the major degraders of DMSP, using two known pathways: demethylation and cleavage.Many phytoplankton and some fungi can also cleave DMSP. So far seven different prokaryotic and one eukaryotic DMSP lyases have been identified. This review describes the global distribution pattern of DMSP and DMS, the known genes for biosynthesis and cleavage of DMSP, and the physiological and ecological functions of these important organosulfur molecules, which will improve understanding of the mechanisms of DMSP and DMS production and their roles in the environment.     

Influence of dimethyl sulfide on the carbon cycle and biological production

Dimethyl sulfide (DMS) is a significant source of marine sulfate aerosol and plays an important role in modifying cloud properties. Fully coupled climate simulations using dynamic marine ecosystem and DMS calculations are conducted to estimate DMS fluxes under various climate scenarios and to examine the sign and strength of phytoplankton-DMS-climate feedbacks for the first time. Simulation results show small differences in the DMS production and emissions between pre-industrial and present climate scenarios, except for some areas in the Southern Ocean. There are clear changes in surface ocean DMS concentrations moving into the future, and they are attributable to changes in phytoplankton production and competition driven by complex spatially varying mechanisms. Comparisons between parallel simulations with and without DMS fluxes into the atmosphere show significant differences in marine ecosystems and physical fields. Without DMS, the missing subsequent aerosol indirect effects on clouds and radiative forcing lead to fewer clouds, more solar radiation, and a much warmer climate. Phaeocystis, a uniquely efficient organosulfur producer with a growth advantage under cooler climate states, can benefit from producing the compound through cooling effects of DMS in the climate system. Our results show a tight coupling between the sulfur and carbon cycles. The ocean carbon uptake declines without DMS emissions to the atmosphere. The analysis indicates a weak positive phytoplankton-DMS-climate feedback at the global scale, with large spatial variations driven by individual autotrophic functional groups and complex mechanisms. The sign and strength of the feedback vary with climate states and phytoplankton groups. This highlights the importance of a dynamic marine ecosystem module and the sulfur cycle mechanism in climate projections.     

微生物二甲基巯基丙酸内盐(DMSP)合成途径中关键酶的研究进展

二甲基巯基丙酸内盐(dimethylsulfoniopropionate,DMSP)是全球重要的有机硫化合物之一,参与全球硫循环、信号传递及气候调节。全球DMSP的产量每年高达10⁹ t。DMSP的主要生产者是海洋浮游植物及大型藻类,近年来发现一些海洋细菌也可以产生DMSP,是海洋中DMSP的一个重要来源。目前已报道的DMSP合成途径有3条：甲基化途径、转氨途径和脱羧途径,其中有5种DMSP合成关键酶被鉴定出来。根据近年来的研究成果,本文对DMSP合成过程中关键酶的研究进展进行综述,以期为进一步的研究提供思路。     

Omega-3: a link between global climate change and human health

In recent years, global climate change has been shown to detrimentally affect many biological and environmental factors, including those of marine ecosystems. In particular, global climate change has been linked to an increase in atmospheric carbon dioxide, UV irradiation, and ocean temperatures, resulting in decreased marine phytoplankton growth and reduced synthesis of omega-3 polyunsaturated fatty acids (PUFAs). Marine phytoplankton are the primary producers of omega-3 PUFAs, which are essential nutrients for normal human growth and development and have many beneficial effects on human health. Thus, these detrimental effects of climate change on the oceans may reduce the availability of omega-3 PUFAs in our diets, exacerbating the modern deficiency of omega-3 PUFAs and imbalance of the tissue omega-6/omega-3 PUFA ratio, which have been associated with an increased risk for cardiovascular disease, cancer, diabetes, and neurodegenerative disease. This article provides new insight into the relationship between global climate change and human health by identifying omega-3 PUFA availability as a potentially important link, and proposes a biotechnological strategy for addressing the potential shortage of omega-3 PUFAs in human diets resulting from global climate change.     

Recent insights into oceanic dimethylsulfoniopropionate biosynthesis and catabolism

Dimethylsulfoniopropionate (DMSP), a globally important organosulfur compound is produced in prodigious amounts (2.0 Pg sulfur) annually in the marine environment by phytoplankton, macroalgae, heterotrophic bacteria, some corals and certain higher plants. It is an important marine osmolyte and a major precursor molecule for the production of climate-active volatile gas dimethyl sulfide (DMS). DMSP synthesis take place via three pathways: a transamination ‘pathway-’ in some marine bacteria and algae, a Met-methylation ‘pathway-’ in angiosperms and bacteria and a decarboxylation ‘pathway-’ in the dinoflagellate, Crypthecodinium. The enzymes DSYB and TpMMT are involved in the DMSP biosynthesis in eukaryotes while marine heterotrophic bacteria engage key enzymes such as DsyB and MmtN. Several marine bacterial communities import DMSP and degrade it via cleavage or demethylation pathways or oxidation pathway, thereby generating DMS, methanethiol, and dimethylsulfoxonium propionate, respectively. DMSP is cleaved through diverse DMSP lyase enzymes in bacteria and via Alma1 enzyme in phytoplankton. The demethylation pathway involves four different enzymes, namely DmdA, DmdB, DmdC and DmdD/AcuH. However, enzymes involved in the oxidation pathway have not been yet identified. We reviewed the recent advances on the synthesis and catabolism of DMSP and enzymes that are involved in these processes.     

Phytoplankton decline in the eastern North Pacific transition zone associated with atmospheric blocking

Global climate change can significantly influence oceanic phytoplankton dynamics, and thus biogeochemical cycles and marine food webs. However, associative explanations based on the correlation between chlorophyll‐a concentration (Chl‐a) and climatic indices is inadequate to describe the mechanism of the connection between climate change, large‐scale atmospheric dynamics, and phytoplankton variability. Here, by analyzing multiple satellite observations of Chl‐a and atmospheric conditions from National Center for Environmental Prediction/National Center for Atmospheric Research reanalysis datasets, we show that high‐latitude atmospheric blocking events over Alaska are the primary drivers of the recent decline of Chl‐a in the eastern North Pacific transition zone. These blocking events were associated with the persistence of large‐scale atmosphere pressure fields that decreased westerly winds and southward Ekman transport over the subarctic ocean gyre. Reduced southward Ekman transport leads to reductions in nutrient availability to phytoplankton in the transition zone. The findings describe a previously unidentified climatic factor that contributed to the recent decline of phytoplankton in this region and propose a mechanism of the top‐down teleconnection between the high‐latitude atmospheric circulation anomalies and the subtropical oceanic primary productivity. The results also highlight the importance of understanding teleconnection among atmosphere–ocean interactions as a means to anticipate future climate change impacts on oceanic primary production.     

The neuroecology of dimethyl sulfide: a global-climate regulator turned marine infochemical

Information transfer influences food-web dynamics in the marine environment, but infochemicals involved in these processes are only beginning to be understood. Dimethylsulfoniopropionate (DMSP) is produced by phytoplankton and other marine algae, and has been studied primarily in the context of sulfur cycling and regulation of global climate. My laboratory has been investigating DMSP and its breakdown product, dimethyl sulfide as infochemicals associated with trophic interactions in marine habitats, including sub-Antarctic and coral reef ecosystems. Using a neuroecological approach, our work has established that these biogenic sulfur compounds serve as critical signal molecules in marine systems and provides us with a more mechanistic understanding of how climate change may impact information transfer within marine food webs.     

Aluminum effects on marine phytoplankton: implications for a revised Iron Hypothesis (Iron–Aluminum Hypothesis)

In contrast to substantial studies and established knowledge of aluminum (Al) effects (mainly toxicity) on freshwater organisms and terrestrial plants, and even on human health, only a few studies of Al effects on marine organisms have been reported, and our understanding of the role of Al in marine biogeochemistry is limited. In this paper, we review the results of both field and laboratory experiments on the effects of Al on marine organisms, including Al toxicity to marine phytoplankton and the beneficial effects of Al on marine phytoplankton growth, and we discuss possible links of Al to the biological pump and the global carbon cycle. We propose a revised Iron (Fe) Hypothesis, i.e., the Fe–Al Hypothesis that introduces the idea that Al as well as Fe play an important role in the glacial-interglacial change in atmospheric CO₂ concentrations and climate change. We propose that Al could not only facilitate Fe utilization, dissolved organic phosphorus utilization and nitrogen fixation by marine phytoplankton, enhancing phytoplankton biomass and carbon fixation in the upper oceans, but also reduce the decomposition and decay of biogenic matter. As a result, Al allows potentially more carbon to be exported and sequestered in the ocean depths through the biological pump. We also propose that Al binds to superoxide to form an Al-superoxide complex, which could catalyze the reduction of Fe(III) to Fe(II) and thus facilitate Fe utilization by marine phytoplankton and other microbes. Further ocean fertilization experiments with Fe and Al are suggested, to clarify the role of Al in the stimulation of phytoplankton growth and carbon sequestration in the ocean depths.     

EXPERIMENTAL EVOLUTION MEETS MARINE PHYTOPLANKTON

Our perspective highlights potentially important links between disparate fields—biological oceanography, climate change research, and experimental evolutionary biology. We focus on one important functional group—photoautotrophic microbes (phytoplankton), which are responsible for ～50% of global primary productivity. Global climate change currently results in the simultaneous change of several conditions such as warming, acidification, and nutrient supply. It thus has the potential to dramatically change phytoplankton physiology, community composition, and may result in adaptive evolution. Although their large population sizes, standing genetic variation, and rapid turnover time should promote swift evolutionary change, oceanographers have focussed on describing patterns of present day physiological differentiation rather than measure potential adaptation in evolution experiments, the only direct way to address whether and at which rate phytoplankton species will adapt to environmental change. Important open questions are (1) is adaptation limited by existing genetic variation or fundamental constraints? (2) Will complex ecological settings such as gradual versus abrupt environmental change influence adaptation processes? (3) How will increasing environmental variability affect the evolution of phenotypic plasticity patterns? Because marine phytoplankton species display rapid acclimation capacity (phenotypic buffering), a systematic study of reaction norms renders them particularly interesting to the evolutionary biology research community.     

TROPHIC INTERACTIONS IN THE SEA: AN ECOLOGICAL ROLE FOR CLIMATE RELEVANT VOLATILES?1

When attacked by herbivores, land plants can produce a variety of volatile compounds that attract carnivorous mutualists. Plants and carnivores can benefit from this symbiotic relationship, because the induced defensive interaction increases foraging success of the carnivores, while reducing the grazing pressure exerted by the herbivores on the plants. Here, we examine whether aquatic phytoplankton use volatile chemical cues in analogous tritrophic interactions. Marine algae produce several classes of biogenic gases such as non‐methane hydrocarbons, organohalogens, ammonia and methylamines, and dimethylsulfide. The grazing‐induced release of marine biogenic volatiles is poorly understood, however, and its effect on the chemical ecology of plankton and the foraging behavior of predators is essentially unknown. We outline grazing‐induced defenses in algae and highlight the biogenic production of volatiles when phytoplankton are attacked by herbivores. The role of chemical signaling in marine ecology presents several possible avenues for future research, and we believe that progress in this area will result in better understanding of species competition, bloom development, and the structuring of food webs in the sea. This has further implications for biogeochemical cycles, because several key compounds are emitted that influence the chemistry of the atmosphere and global climate.     

10种常见甲藻细胞体积与细胞碳、氮含量的关系

选择10种常见甲藻,通过构建相应细胞几何模拟图形从而计算了每种甲藻细胞的体积,利用元素分析仪测定了每种甲藻的单个细胞碳、氮含量,并分析了细胞体积与细胞碳、氮含量之间的关系。结果表明,10种常见甲藻的细胞体积差异显著,最小仅为2.97×10² μm³(卡特双甲藻),最大可达到4.50×10⁴ μm³(红色赤潮藻),相差2个数量级;单个细胞碳、氮含量变化范围分别为54.50-2238.00 pg/个和11.42-482.28 pg/个,均相差40多倍。细胞体积与单个细胞碳、氮含量存在极显著的正相关线性关系(P<0.0001)。     

Effects of climate‐driven primary production change on marine food webs: implications for fisheries and conservation

Climate change is altering the rate and distribution of primary production in the world's oceans. Primary production is critical to maintaining biodiversity and supporting fishery catches, but predicting the response of populations to primary production change is complicated by predation and competition interactions. We simulated the effects of change in primary production on diverse marine ecosystems across a wide latitudinal range in Australia using the marine food web model Ecosim. We link models of primary production of lower trophic levels (phytoplankton and benthic producers) under climate change with Ecosim to predict changes in fishery catch, fishery value, biomass of animals of conservation interest, and indicators of community composition. Under a plausible climate change scenario, primary production will increase around Australia and generally this benefits fisheries catch and value and leads to increased biomass of threatened marine animals such as turtles and sharks. However, community composition is not strongly affected. Sensitivity analyses indicate overall positive linear responses of functional groups to primary production change. Responses are robust to the ecosystem type and the complexity of the model used. However, model formulations with more complex predation and competition interactions can reverse the expected responses for some species, resulting in catch declines for some fished species and localized declines of turtle and marine mammal populations under primary productivity increases. We conclude that climate‐driven primary production change needs to be considered by marine ecosystem managers and more specifically, that production increases can simultaneously benefit fisheries and conservation. Greater focus on incorporating predation and competition interactions into models will significantly improve the ability to identify species and industries most at risk from climate change.     

Single-taxon field measurements of bacterial gene regulation controlling DMSP fate

The ‘bacterial switch'' is a proposed regulatory point in the global sulfur cycle that routes dimethylsulfoniopropionate (DMSP) to two fundamentally different fates in seawater through genes encoding either the cleavage or demethylation pathway, and affects the flux of volatile sulfur from ocean surface waters to the atmosphere. Yet which ecological or physiological factors might control the bacterial switch remains a topic of considerable debate. Here we report the first field observations of dynamic changes in expression of DMSP pathway genes by a single marine bacterial species in its natural environment. Detection of taxon-specific gene expression in Roseobacter species HTCC2255 during a month-long deployment of an autonomous ocean sensor in Monterey Bay, CA captured in situ regulation of the first gene in each DMSP pathway (dddP and dmdA) that corresponded with shifts in the taxonomy of the phytoplankton community. Expression of the cleavage pathway was relatively greater during a high-DMSP-producing dinoflagellate bloom, and expression of the demethylation pathway was greater in the presence of a mixed diatom and dinoflagellate community. These field data fit the prevailing hypothesis for bacterial DMSP gene regulation based on bacterial sulfur demand, but also suggest a modification involving oxidative stress response, evidenced as upregulation of catalase via katG, when DMSP is demethylated.     

INTRACELLULAR DIMETHYLSULFOXIDE (DMSO) IN UNICELLULAR MARINE ALGAE: SPECULATIONS ON ITS ORIGIN AND POSSIBLE BIOLOGICAL ROLE

Recent studies have established that aqueous phase concentrations of dimethylsulfoxide (DMSO) often exceed those of dimethylsulfoniopropionate (DMSP) and dimethylsulfide (DMS). Yet, in comparison to DMSP and DMS, DMSO remains a poorly understood component of the marine sulfur cycle. Much of what is known about the mechanisms for the formation and loss for DMSO is inferred from laboratory experiments, and no explanation exists to rationalize how a large pool of DMSO is maintained. One formation pathway that, until very recently, has been ignored involves the direct synthesis of DMSO by marine phytoplankton. This review examines some of the circumstantial evidence for DMSO in marine particulate material and recent reports containing preliminary data for particulate DMSO (DMSO_p) in the marine environment. Drawing on literature from a range of scientific disciplines, speculations on the possible origins and biological functions of intracellular DMSO are also made. On the basis of its physicochemical properties, intracellular DMSO could have a potential role as a cryoprotectant, a specialist cryo-osmoregulator in extreme environments, an intracellular electrolyte modifier, and a free-radical scavenger. The review also assesses the impact of DMSO_p at both the organism and the global level. Consideration is given to the marine biogeochemical cycling of sulfur and potential links to climate control.     

Sulfur and primary production in aquatic environments: an ecological perspective

Sulfur is one of the critical elements in living matter, as it participates in several structural, metabolic and catalytic activities. Photosynthesis is an important process that entails the use of sulfur during both the light and carbon reactions. Nearly half of global photosynthetic carbon fixation is carried out by phytoplankton in the aquatic environment. Aquatic environments are very different from one another with respect to sulfur content: while in the oceans sulfate concentration is constantly high, freshwaters are characterized by daily and seasonal variations and by a wide range of sulfur concentration. The strategies that algal cells adopt for energy and resource allocation often reflect these differences. In the oceans, the amount and chemical form of sulfur has changed substantially during the course of the Earth's history; it is possible that sulfur availability played a role in the evolution of marine phytoplankton communities and it may continue to have appreciable effects on global biogeochemistry and ecology. Phytoplankton is also the main biogenic source of sulfur; sulfur can be released into the atmosphere by algal cells as dimethylsulfide, with possibly important repercussions on global climate. These and related matters are discussed in this review.     

Sulfur and phytoplankton: acquisition, metabolism and impact on the environment

Sulfur emission from marine phytoplankton has been recognized as an important factor for global climate and as an entry into the biogeochemical S cycle. Despite this significance, little is known about the cellular S metabolism in algae that forms the basis of this emission. Some biochemical and genetic evidence for regulation of S uptake and assimilation is available for the freshwater model alga Chlamydomonas. However, the marine environment is substantially different from most fresh waters, containing up to 50 times higher free sulfate concentrations and challenging the adaptive mechanisms of primary and secondary S metabolism in marine algae. This review intends to integrate ecological and physiological data to provide a comprehensive view of the role of S in the oceans.     

Abundance and function of bacteria in the Southern Ocean.

The very low water temperatures existing in polar oceans that experience seasonal advance and retreat of pack ice do not inhibit the presence of large bacterial populations. Bacteria may contribute significantly to the energy transfers within the Southern Ocean. In the last decades, notable progress has been made in the knowledge of the role of marine bacteria in the Southern Ocean. A short overview of the abundance and function ofAntarctic marine bacteria is given, with respect to metabolic activity. The importance of spatial and temporal variability is described. The ecological function of Antarctic marine bacterioplankton is discussed. Depending on food web structure, bacteria may be either a link in food webs supporting metazoan production, or a sink where bacterial production is metabolised by microorganisms. In the more oligotrophic areas and during certain periods of the year bacterial biomass dominates phytoplankton. The microbial food web is therefore the dominant pathway for carbon and energy flow in Antarctic seawater.     

Soil respiration partitioning in afforested temperate peatlands

Large marine regions, including the exceptionally productive Southern Ocean, are iron-limited. As a result, there has been substantial interest in iron-fertilizing high nutrient low chlorophyll (HNLC) areas in an effort to sequester atmospheric carbon dioxide. More recently, research has shifted to quantifying the beneficial effects of iron recycling by marine biota. Marine top predators such as whales and seabirds have been examined specifically in this regard as they have high biomass, form dense aggregations, and excrete bioavailable iron in concentrations seven orders of magnitude higher than ambient seawater. Despite it being well established that marine fauna link the iron and carbon cycles, the connection of this process to the sulfur cycle has rarely been considered. The chemoattraction of specific marine fauna to algal-derived dimethyl sulfide (DMS) is key in triggering dense, multi-species foraging aggregations that induce iron recycling, augmenting carbon assimilation. The goal of this paper is twofold; first, to highlight DMS chemoattraction as a behavior that catalyzes carbon sequestration via natural iron fertilization, and second, to identify knowledge gaps that recent biogeochemical advances can address. Fostering this interdisciplinary research will enhance our understanding of global climate regulation, ecosystem services provided by marine top predators, and the biogeochemical cycles of carbon, iron, and sulfur in HNLC waters.     

Production of volatile sulfur compounds during the decomposition of algal mats.

Blue-green algal mats incubated anaerobically rapidly produce large amounts of volatile sulfur compounds, including hydrogen sulfide, methyl mercaptan, and dimethyl sulfide. The major organic sulfur compound is methyl mercaptan, in contrast to previous results with marine eucaryotic algae. Light inhibited production of volatile sulfur compounds, apparently because the algae then produced O2, rendering the system aerobic.     

Production of volatile sulfur compounds during the decomposition of algal mats.

Blue-green algal mats incubated anaerobically rapidly produce large amounts of volatile sulfur compounds, including hydrogen sulfide, methyl mercaptan, and dimethyl sulfide. The major organic sulfur compound is methyl mercaptan, in contrast to previous results with marine eucaryotic algae. Light inhibited production of volatile sulfur compounds, apparently because the algae then produced O2, rendering the system aerobic.