Microbial controls on DMSP degradation and DMS formation in the Sargasso Sea

Bacterial degradation of dimethylsulfoniopropionate (DMSP) represents one of the main sources of the climatically–active trace gas dimethylsulfide (DMS) in the upper ocean. Short-term enrichment studies to stimulate specific pathways of DMSP degradation in oligotrophic waters from the Sargasso Sea were used to explore regulatory connections between the different bacterial DMSP degradation steps and determine potential biological controls on DMS formation in the open ocean. Experiments were conducted with surface water at the BATS station in the western North Atlantic Ocean. We added selected organic substrates (25 nmol L^?1 final concentration) to induce different steps of DMSP degradation in the microbial community, and then measured DMSP dynamics (assimilation and turnover rates), DMS yields (using ³⁵sulfur-DMSP tracer), and bacterial production rates. In most treatments, the main fate of consumed S-DMSP was excretion as a non-volatile S product. ³⁵S-DMSP tracer turnover rates (accumulation + assimilation + excretion of transformed products as DMS or others) increased upon addition of DMSP and glucose, but not acrylate, methymercaptopropionate (MMPA), methanethiol, DMS or glycine betaine. DMS yields from ³⁵S-DMSP never exceeded 16 % except in a short term DMSP enrichment, for which the yield reached 45 % (±17 %). Results show that availability of non-sulfur containing labile C sources (glucose, acrylate) decreased bacterial DMS production while stimulating bacterial heterotrophic production, and suggest an influence of bacterial sulfur demand in controlling DMS-yielding pathways. However, regulatory effects on ³⁵S-DMSP fate were not consistent across all reduced sulfur compounds (i.e., methanethiol or MMPA), and may reflect alternate roles of DMSP as a bacterial energy source and osmolyte.     

Effect of iron on phytoplankton production in the Sargasso Sea

Addition of chelated iron at concentrations of 0.5, 1.0, 10 and 100μg Fe·l^?1 to Sargasso Sea phytoplankton assemblages did not affect the rate of photosynthesis during 4-h incubation experiments. In experiments with 72-h incubations, however, iron enhanced carbon assimilation. The enhancement was independent of iron concentration.     

Hydrogen production potential of fermentative microorganisms from the Sargasso Sea

Mounting evidence suggests that ammonia-oxidizing archaea (AOA) may play important roles in nitrogen cycling in geothermal environments. In this study, the diversity, distribution and ecological significance of AOA in terrestrial hot springs in Kamchatka (Far East Russia) were explored using amoA genes complemented by analysis of glycerol dialkyl glycerol tetraethers (GDGTs) of archaea. PCR amplification of functional genes (amoA) from AOA and ammonia-oxidizing bacteria (AOB) was performed on microbial mats/streamers and sediments collected from three hot springs (42°C to 87°C and pH 5.5-7.0). No amoA genes of AOB were detected. The amoA genes of AOA formed three distinct phylogenetic clusters with Cluster 3 representing the majority (～59%) of OTUs. Some of the sequences from Cluster 3 were closely related to those from acidic soil environments, which is consistent with the predominance of low pH (<7.0) in these hot springs. Species richness (estimated by Chao1) was more frequently higher at temperatures below 75°C than above it, indicating that AOA may be favored in the moderately high temperature environments. Quantitative PCR of 16S rRNA genes showed that crenarchaeota counted for up to 80% of total archaea. S-LIBSHUFF separated all samples into two phylogenetic groups. The profiles of GDGTs were well separated among the studied springs, suggesting a spatial patterning of archaeal lipid biomarkers. However, this patterning did not correlate significantly with variation in archaeal amoA, suggesting that AOA are not the predominant archaeal group in these springs producing the observed GDGTs.     

Picoeukaryotic sequences in the Sargasso Sea metagenome

Background  

With genome sequencing becoming more and more affordable, environmental shotgun sequencing of the microorganisms present in an environment generates a challenging amount of sequence data for the scientific community. These sequence data enable the diversity of the microbial world and the metabolic pathways within an environment to be investigated, a previously unthinkable achievement when using traditional approaches. DNA sequence data assembled from extracts of 0.8 μm filtered Sargasso seawater unveiled an unprecedented glimpse of marine prokaryotic diversity and gene content. Serendipitously, many sequences representing picoeukaryotes (cell size <2 μm) were also present within this dataset. We investigated the picoeukaryotic diversity of this database by searching sequences containing homologs of eight nuclear anchor genes that are well conserved throughout the eukaryotic lineage, as well as one chloroplastic and one mitochondrial gene.     

The microbial selenoproteome of the Sargasso Sea

Background  

Selenocysteine (Sec) is a rare amino acid which occurs in proteins in major domains of life. It is encoded by TGA, which also serves as the signal for termination of translation, precluding identification of selenoprotein genes by available annotation tools. Information on full sets of selenoproteins (selenoproteomes) is essential for understanding the biology of selenium. Herein, we characterized the selenoproteome of the largest microbial sequence dataset, the Sargasso Sea environmental genome project.     

Response of Sargasso Sea phytoplankton biomass, growth rates and primary production to seasonally varying physical forcing

The response of phytoplankton biomass, growth rates and primaryproduction to seasonally varying physical forcing was studiedat a station southeast of Bermuda over an 18 month period. Phytoplanktongrowth rates and primary production were measured using thepigment-labeling method, and phytoplankton biomass was calculatedfrom these measurements. Phytoplankton carbon biomass variedsystematically over the year. Highest values were observed duringthe winter and spring. Seasonal variations of chlorophyll (Chi)a in the surface layer could primarily be attributed to variationsin phytoplankton biomass and secondarily to photoacclimation.During the summer period, average values of carbon (C)/Chl ratios(g C g^–1 Chi) ranged from 160 at the surface to 33 atthe 1.6% light level, changes attributed to photoacclimationof the phytoplankton, consistent with the observation that phytoplanktonbiomass did not vary as a function of depth. Phytoplankton growthrates in the surface layer did not vary systematically overthe year, ranging from 0.15 to 0.45 day^–1, in spite ofseasonally varying concentrations of nitrate. Growth rates variedas a function of depth from average values of 0.3 day^–1in the surface layer to <0.1 day¹ at the 1.6% light level.Thus, the primary response of the phytoplankton community tonutrient enrichment during the winter period was an increasein phytoplankton biomass rather than an increase in growth rates.A simple nutrient-phyto-plankton-zooplankton model was usedto explore this phenomenon. The model demonstrated that theobserved response of the phytoplankton to nutrient enrichmentis only possible when phytoplankton growth is not severely limitedby nutrients.     

Vertical distribution of picoeukaryotic diversity in the Sargasso Sea

Eukaryotic molecular diversity within the picoplanktonic size-fraction has primarily been studied in marine surface waters. Here, the vertical distribution of picoeukaryotic diversity was investigated in the Sargasso Sea from euphotic to abyssal waters, using size-fractionated samples (< 2 microm). 18S rRNA gene clone libraries were used to generate sequences from euphotic zone samples (deep chlorophyll maximum to the surface); the permanent thermocline (500 m); and the pelagic deep-sea (3000 m). Euphotic zone and deep-sea data contrasted strongly, the former displaying greater diversity at the first-rank taxon level, based on 232 nearly full-length sequences. Deep-sea sequences belonged almost exclusively to the Alveolata and Radiolaria, while surface samples also contained known and putative photosynthetic groups, such as unique Chlorarachniophyta and Chrysophyceae sequences. Phylogenetic analyses placed most Alveolata and Stramenopile sequences within previously reported 'environmental' clades, i.e. clades within the Novel Alveolate groups I and II (NAI and NAII), or the novel Marine Stramenopiles (MAST). However, some deep-sea NAII formed distinct, bootstrap supported clades. Stramenopiles were recovered from the euphotic zone only, although many MAST are reportedly heterotrophic, making the observed distribution a point for further investigation. An unexpectedly high proportion of radiolarian sequences were recovered. From these, five environmental radiolarian clades, RAD-I to RAD-V, were identified. RAD-IV and RAD-V were composed of Taxopodida-like sequences, with the former solely containing Sargasso Sea sequences, although from all depth zones sampled. Our findings highlight the vast diversity of these protists, most of which remain uncultured and of unknown ecological function.     

Effect of UV- radiation on DMSP content and DMS formation of Phaeocystis antarctica

DMSP (dimethyl sulphonium propionate) contents produced by an Antarctic marine phytoplankton species, Phaeocystis antarctica (Prymnesiophyta), which were incubated under light conditions with radiations of different UV wavebands, were measured by gas chromatography after various exposure times. Full light (UV-B + UV-A + PAR) caused the strongest decrease in the production of DMSP in the alga. A marked depression of DMSP content was also observed with short UV-B and UV-A wavebands after 3 h. It was therefore hypothesised that DMSP production in Phaeocystis antarctica was inhibited by UV radiation. There was a negative correlation on change of DMSP contents under UV radiation. There was a negative correlation on change of DMSP contents under UV radiation with exposure times. The conversion rate of DMSP dissolved to DMS (dimethyl sulphide) was significantly increased with UV radiation. The possibility could not be excluded that a high concentration of free chemical radicals in seawater due to UV radiation resulted in an increase of DMSP cleavage in seawater. The oxidation of DMS in seawater due to UV-B radiation could result in a decrease of its flux to the atmosphere. The effect of UV radiation on DMSP production and oxidation of DMS may be an important factor in the variability of DMSP and the global flux of DMS from ocean to atmosphere. Received: 17 June 1996 / Accepted: 17 July 1997     

Metabolism of DMSP, DMS and DMSO by the cultivable bacterial community associated with the DMSP-producing dinoflagellate Scrippsiella trochoidea

Bacterial species associated with the dimethylsulfoniopropionate (DMSP)-producing phytoplankton Scrippsiella trochoidea were cultured and identified, with the aim of establishing their ability to metabolise DMSP, dimethylsulfide (DMS) and dimethylsulfoxide (DMSO). Results demonstrate that of the cultivable bacteria only α-Proteobacteria were capable of producing DMS from DMSP. The concentration of DMSP was shown to affect the amount of DMS produced. Lower DMSP concentrations (1.5?μmol?dm^?3) were completely assimilated, whereas higher concentrations (10?μmol?dm^?3) resulted in increasing amounts of DMS being produced. By contrast to the restricted set of bacteria that metabolised DMSP,?~?70% of the bacterial isolates were able to ‘consume’ DMS. However, 98-100% of the DMS removed was accounted for as DMSO. Notably, a number of these bacteria would only oxidise DMS in the presence of glucose, including members of the γ-Proteobacteria and Bacteroidetes. The observations from this study, coupled with published field data, identify DMS oxidation to DMSO as a major transformation pathway for DMS, and we speculate that the fate of DMS and DMSP in the field are tightly coupled to the available carbon produced by phytoplankton.     

Environmental drivers of sardine (Sardina pilchardus) in the Catalan Sea (NW Mediterranean Sea)

In the area surrounding the Ebro Delta, similar to the rest of the north-western Mediterranean Sea, the sardine (Sardina pilchardus), one of the most exploited small pelagic fishes, has suffered a decreasing trend in abundance and biomass in the last decade, with low values in evidence since 2007. The dependence of this species on environmental factors makes it vulnerable to environmental changes; consequently, the abundance of the species is highly variable. Using segmented regression, we evaluated the presence of discontinuities in the temporal pattern of the seasonally adjusted landings per unit effort (LPUE), which was used as a proxy for abundance, between 2000 and 2013. The results suggested a sudden increase in mid-2005, followed by a sharp decrease starting in 2006. A generalized additive mixed model (GAMM), incorporating the linear correlation structure, was used to identify relationships between the seasonally adjusted LPUE and trends of the Western Mediterranean Oscillation index (WeMOI), sea surface temperature (SST), salinity (SAL) and the Zonal and Meridional Currents (ZC and MC, respectively). The variance inflation factors (VIFs) were calculated between all environmental variables to avoid high-dimensional collinearities. The final GAMM, selected using the Akaike information criterion, indicated that positive WeMOI values, which favour the productivity of the area, along with SAL (at ca. 38) and a northward-flowing MC, favoured LPUE. Our results, obtained by applying a method in which variation due to season, non-linearity, autocorrelation and collinearity of the covariates was taken into account, provided further evidence of the dependence of the sardine population upon specific hydrographic variables.     

Studies on the small invertebrate plankton of the Sargasso Sea

During the German Eel Expedition in Spring 1979, the horizontal and vertical distribution of the invertebrate plankton was studied in the epipelagic zone of the western central Sargasso Sea, based on 55 µm and 100 µm mesh net samples. In the isothermal waters north of the thermal front, plankton biomass was on average 2–3 times higher than in the warmer stratified waters south of the front. With regard to the fraction of small invertebrates (nauplii and microcopepods) the differences in numerical abundance between the two areas were similar to those reported in the literature for other size ranges of organisms. No divergency was obvious in the plankton composition in terms of major taxonomic groups and size classes. In both parts of the area, organisms smaller than 400 µm, which form a fraction not quantitatively sampled by the conventional 200 µm or 300 µm mesh nets, accounted for 71–92 % of the total number of organisms in the 55 µm net samples and for more than 50 % in the 100 µm net samples. Average concentrations of the potential food supply for early larval fish stages in the upper 100 m appear to be comparable with values reported in the literature for areas well known for larval fish development, such as the California Current.     

Distribution ofSargassum natans and some of its epibionts in the Sargasso Sea

Sargassum was collected during the Sargasso Sea Eel Expedition in Spring 1979. On average, the morphological form typeSargassum natans (I) made up 85 % of the total wet weight of the samples. South of the thermal front, larger amounts of weeds were observed. Here, the bladder size ofS. natans (I) was significantly smaller (surface 47±7 mm²) than in the northern part (surface: 64±15 mm²), while phylloids showed no differences. The composition and density of some epibionts were examined.Membranipora tuberculata (Bryozoa),Clytia noliformis (Hydrozoa) and the calcarious algae Melobesia sp. (Rhodophyta) were studied quantitatively according to different features at 17 stations.M. tuberculata was the most abundant epibiont followed byC. noliformis. Compared with these species, "Melobesia sp." occurred in considerably lower quantities.M. tuberculata showed a preference for bladders rather than phylloids;C. noliformis was found more frequently on phylloids than on bladders. "Melobesia sp." did not show any preference. Frequency and abundance of these epibionts were higher north of the thermal front than south of this front. North of the frontS. natans (I) was less abundant but bladders were larger.     

Diversity of DMSP transport in marine bacteria, revealed by genetic analyses

The enzyme product of the dddD gene, found in several different marine bacteria, acts on dimethylsulfoniopropionate (DMSP), liberating dimethyl sulfide (DMS) and generating 3-OH-propionate as the initially detected C3 product. In many bacteria, dddD is near genes whose sequence suggests that they encode a DMSP transporter. These are of two very different types, in the BCCT (betaine-carnitine-choline transporter) family or resembling members of the ABC super-family that import betaines. Even within these two families, the amino acid sequences of these putative transporters are not particularly similar to each other. Genes for the predicted DMSP transporters of Halomonas and Marinomonas (both BCCT type) and of Burkholderia ambifaria AMMD (ABC-type) were each cloned and introduced into an Escherichia coli mutant (MKH13) that is defective in betaine uptake, and so fails to catabolise DMSP even when a cloned dddD gene was present, due to the failure of the substrate to be imported. DMSP-dependent DMS production (Ddd⁺ phenotype) was restored by introducing any of these cloned transporters into MKH13 containing dddD. Other marine bacteria use a range of enzymes, called DddL, DddP, DddQ, DddW and DddY, to cleave DMSP, but the various ddd genes that encode them are usually unlinked to any that are predicted to encode betaine transporters. We identified one gene in Sulfitobacter sp. EE-36 and two in Roseovarius nubinhibens ISM, which, when cloned and introduced into E. coli MKH13, overcame its osmotic sensitivity when it was grown with DMSP or other exogenous betaines. These genes all encoded BCCT transporters, but were unlinked to any known genes involved in DMSP catabolism in these two strains of α-proteobacteria.     

Macroscale patterns of the biological cycling of dimethylsulfoniopropionate (DMSP) and dimethylsulfide (DMS) in the Northwest Atlantic

The influence of the seasonal development of microplankton communities on the cycling of dimethylsulfide (DMS) and its precursor dimethylsulfoniopropionate (DMSP) was investigated along a South–North gradient (36–59^°N) in the Northwest (NW) Atlantic Ocean. Three surveys allowed the sampling of surface mixed layer (SML) waters at stations extending from the subtropical gyre to the Greenland Current during May, July and October 2003. Pools and transformation rates of DMSP and DMS were quantified and related to prevailing physical and biochemical conditions, phytoplankton abundance and taxonomic composition, as well as bacterioplankton abundance and leucine uptake. The South–North progression of the diatom bloom, a prominent feature in the NW Atlantic, did not influence the production of DMS whereas conditions in the N Atlantic Drift lead to a persistent bloom of DMSP-rich flagellate-dominated phytoplankton community and high net DMS production rates. Macroscale patterns of the observed variables were further explored using principal component analysis (PCA). The first axis of the PCA showed a strong association between the spatio-temporal distribution of DMSP and the abundance of several phytoplankton groups including dinoflagellates and prymnesiophytes, as well as with microbial-mediated DMSP_d consumption and yields and rates of the conversion of DMSP into DMS. The second axis revealed a strong association between concentrations of DMS and SML depth and photosynthetically active radiation, a result supporting the prominent role of solar radiation as a driver of DMS dynamics.     

Abundant and diverse bacteria involved in DMSP degradation in marine surface waters

An expanded analysis of oceanic metagenomic data indicates that the majority of prokaryotic cells in marine surface waters have the genetic capability to demethylate dimethylsulfoniopropionate (DMSP). The 1701 homologues of the DMSP demethylase gene, dmdA , identified in the (2007) Global Ocean Sampling (GOS) metagenome, are sufficient for 58% (±9%) of sampled cells to participate in this critical step in the marine sulfur cycle. This remarkable frequency of DMSP-demethylating cells is in accordance with biogeochemical data indicating that marine phytoplankton direct up to 10% of fixed carbon to DMSP synthesis, and that most of this DMSP is subsequently degraded by bacteria via demethylation. The GOS metagenomic data also revealed a new cluster of dmdA sequences (designated Clade E) that implicates marine gammaproteobacteria in DMSP demethylation, along with previously recognized alphaproteobacterial groups Roseobacter and SAR11. Analyses of G+C content and gene order indicate that lateral gene transfer is likely responsible for the wide distribution of dmdA among diverse taxa, contributing to the homogenization of biogeochemical roles among heterotrophic marine bacterioplankton. Candidate genes for the competing bacterial degradation process that converts DMSP to the climate-active gas dimethylsulfide (DMS) ( dddD and dddL ) occur infrequently in the (2007) GOS metagenome, suggesting either that the key DMS-producing bacterial genes are yet to be identified or that DMS formation by free-living bacterioplankton is insignificant relative to their demethylation activity.     

An analysis of the Sargasso Sea resource and the consequences for database composition

Background  

The environmental sequencing of the Sargasso Sea has introduced a huge new resource of genomic information. Unlike the protein sequences held in the current searchable databases, the Sargasso Sea sequences originate from a single marine environment and have been sequenced from species that are not easily obtainable by laboratory cultivation. The resource also contains very many fragments of whole protein sequences, a side effect of the shotgun sequencing method.     

Organisms associated with stimulated epipelagic bioluminescence in the Sargasso Sea and the Gulf Stream

On three cruises, vertical profiles of stimulated bioluminescencewere measured during the late evening in the upper 200 m ofthe Sargasso Sea using a submarine photometer. On one cruise,organisms were collected in a 25 µm porosity net afterpassing through the photometer where the intensity and lightcontent of their bioluminescence were recorded. Correlationsof bioluminescence and organisms suggested that the majorityof the stimulated bioluminescence produced in the Sargasso Seawas from zooplankton: crustaceans (ostracods, copepods, copepodlarvae, euphausid larvae), larvaceans and colonial radiolarians.In addition, the photosynthetic dinoflagellate Pyrocystis noctilucaappeared to produce 5–30% of the measured bioluminescenceat some stations. Other dinoflagellates, although numerous,were dim and thus produced less than a few percent of the stimulatedbioluminescent light. The subsurface peaks in the Gulf Streamand northern Sargasso Sea were due primarily to ostracods andlarvaceans. In the Anegada Passage in October, and in the northernSargasso Sea and the Gulf Stream in August, there were pronouncedsubsurface peaks in bioluminescence associated with the thermocline.In Anegada Passage and the Sargasso Sea just north of PuertoRico in October, and in the Gulf Stream in August, the subsurfacebioluminescence peak was in or slightly above the chlorophyllmaximum. However, at the Sargasso Sea stations in August, itwas 10–40 m above the depth of the chlorophyll maximum.