Algal blooms produce large amounts of dimethyl sulfide (DMS), a volatile with a diverse signaling role in marine food webs that is emitted to the atmosphere, where it can affect cloud formation. The algal enzymes responsible for forming DMS from dimethylsulfoniopropionate (DMSP) remain unidentified despite their critical role in the global sulfur cycle. We identified and characterized Alma1, a DMSP lyase from the bloom-forming algae Emiliania huxleyi. Alma1 is a tetrameric, redox-sensitive enzyme of the aspartate racemase superfamily. Recombinant Alma1 exhibits biochemical features identical to the DMSP lyase in E. huxleyi, and DMS released by various E. huxleyi isolates correlates with their Alma1 levels. Sequence homology searches suggest that Alma1 represents a gene family present in major, globally distributed phytoplankton taxa and in other marine organisms.
Dimethyl sulfide (DMS) is produced in oceans in vast amounts (>10(7) tons/year) and mediates a wide range of processes from regulating marine life forms to cloud formation. Nonetheless, none of the enzymes that produce DMS from dimethylsulfoniopropionate (DMSP) has been adequately characterized. We describe the expression and purification of DddD from the marine bacterium Marinomonas sp. MWYL1 and its biochemical characterization. We identified DMSP and acetyl-coenzyme A to be DddD's native substrates and Asp602 as the active site residue mediating the CoA-transferase prior to lyase activity. These findings shed light on the biochemical utilization of DMSP in the marine environment.
The sinking of organic particles in the ocean and their degradation by marine microorganisms is one of the main drivers of one of the most conspicuous carbon fluxes on Earth, the biological pump [1][2][3][4][5][6][7] . Yet, the mechanisms determining the magnitude of the pump remain poorly understood, limiting our ability to predict this carbon flux in future ocean scenarios. Current ocean models assume that the biological pump is governed by the competition between sinking speed and degradation rate, with the two processes independent from one another [8][9][10][11] . Contrary to this paradigm, we show that sinking itself is a primary determinant of the rate at which bacteria degrade particles. Heterotrophic bacterial degradation rates were obtained from a laboratory study on model surfacecolonized particles at atmospheric pressure under a range of flow speeds to mimic different sinking velocities. We find that even modest sinking speeds of 8 m/day enhance degradation rates more than 10-fold compared to degradation rates of non-sinking particles. We discovered that the molecular mechanism underlying this sinking-enhanced degradation is the flow-induced removal of the oligomeric breakdown products from the particles, which otherwise compete for enzymatic activity. This mechanism applies across several substrates and bacterial strains, suggesting it could potentially occur more broadly under natural marine conditions. Integrating our findings into a mathematical model of vertical particulate carbon flux, we show that the coupling of sinking and degradation may contribute, in conjunction with other processes, to determine the magnitude of the vertical carbon flux in the ocean.The biological pump is the process by which CO2 from the atmosphere is converted by marine photosynthetic organisms into biomass and inorganic carbonate shells, which undergo aggregation when those cells die to form 'marine snow' particles that sink to the ocean depth [3][4][5] .Several processes that vary in magnitude with site, depth and season concurrently affect the sinking of particles and the vertical export of the carbon present in marine snow. These processes
Marine organisms release dimethylsulfide (DMS) via cleavage of dimethylsulfoniopropionate (DMSP). Different genes encoding proteins with DMSP lyase activity are known, yet these exhibit highly variable levels of activity. Most assigned bacterial DMSP lyases, including DddK, DddL, DddQ, DddW, and DddY, appear to belong to one, cupin-like superfamily. Here, we attempted to define and map this superfamily dubbed cupin-DLL (DMSP lyases and lyase-like). To this end, we have pursued the characterization of various recombinant DMSP lyases belonging to this superfamily of metalloenzymes, and especially of DddY and DddL that seem to be the most active DMSP lyases in this superfamily. We identified two conserved sequence motifs that characterize this superfamily. These motifs include the metal-ligating residues that are absolutely essential and other residues including an active site tyrosine that seems to play a relatively minor role in DMSP lysis. We also identified a transition metal chelator, N, N, N', N'-tetrakis(2-pyridylmethyl)ethane-1,2-diamine (TPEN), that selectively inhibits all known members of the cupin-DLL superfamily that exhibit DMSP lyase activity. A phylogenetic analysis indicated that the known DMSP lyase families are sporadically distributed suggesting that DMSP lyases evolved within this superfamily multiple times. However, unusually low specific DMSP lyase activity and genome context analysis suggest that DMSP lyase is not the native function of most cupin-DLL families. Indeed, a systematic profiling of substrate selectivity with a series of DMSP analogues indicated that some members, most distinctly DddY and DddL, are bona fide DMSP lyases, while others, foremost DddQ, may only exhibit promiscuous DMSP lyase activity.
Sinking particulate organic carbon out of the surface ocean sequesters carbon on decadal to millennial timescales. Predicting the particulate carbon flux is therefore critical for understanding both global carbon cycling and the future climate. Microbes play a crucial role in particulate organic carbon degradation, but the impact of depth-dependent microbial dynamics on ocean-scale particulate carbon fluxes is poorly understood. Here we scale-up essential features of particle-associated microbial dynamics to understand the large-scale vertical carbon flux in the ocean. Our model provides mechanistic insight into the microbial contribution to the particulate organic carbon flux profile. We show that the enhanced transfer of carbon to depth can result from populations struggling to establish colonies on sinking particles due to diffusive nutrient loss, cell detachment, and mortality. These dynamics are controlled by the interaction between multiple biotic and abiotic factors. Accurately capturing particle-microbe interactions is essential for predicting variability in large-scale carbon cycling.
The ecological interaction between bacteria and sinking particles, such as bacterial degradation of marine snow particles, is regulated by their encounters. Current encounter models focus on the diffusive regime, valid for particles larger than the bacterial run length, yet the majority of marine snow particles are small, and the encounter process is then ballistic. Here, we analytically and numerically quantify the encounter rate between sinking particles and non-motile or motile microorganisms in the ballistic regime, explicitly accounting for the hydrodynamic shear created by the particle and its coupling with micro-organism shape. We complement results with selected experiments on non-motile diatoms. The shape-shear coupling has a considerable effect on the encounter rate and encounter location through the mechanisms of hydrodynamic focusing and screening, whereby elongated micro-organisms preferentially orient normally to the particle surface downstream of the particle (focusing) and tangentially to the surface upstream of the particle (screening). Non-motile elongated micro-organisms are screened from sinking particles because shear aligns them tangentially to the particle surface, which reduces the encounter rate by a factor proportional to the square of the micro-organism aspect ratio. For motile elongated micro-organisms, hydrodynamic focusing increases the encounter rate when particle sinking speed is similar to microorganism swimming speed, whereas for very quickly sinking particles hydrodynamic screening can reduce the encounter rate below that of non-motile micro-organisms. For natural ocean conditions, we connect the ballistic and diffusive limits and compute the encounter rate as a function of shape, motility and particle characteristics. Our results indicate that shear should be taken into account to predict the interactions between bacteria and sinking particles responsible for the large carbon flux in the ocean's biological pump.
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