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COMMENTARY Unifyingchemicalandbiologicalperspectivesof carbonaccumulationintheenvironment Daniel J. Repeta a,1  Heterotrophic microorganisms are fiendishly clever at degrading allshapes andsizes oforganiccompounds to extract the energy they need to build biomass. This distribution of DOM has long been recognized to imply strong feedbacks between DOM production and consumption, but the mechanistic underpinnings of those feedbacks have never been described. At the molecular level, the interaction of DOM supply, microbial uptake and respiration, and microbial community dynamics leads to a bimodal distribution of DOM pools. Other G1 DOM1 DOM2 DOM3 G2 G3 G4 S1 S2 G5 High Productivity High Biomass Rapid cycling High DOM Low productivity Low biomass Slower cycling Low DOM Depth DOM Concentration Fig. [Extracted from the article]

Semi-labile dissolved organic matter (DOM) accumulates in surface waters of the oligotrophic ocean gyres and turns over on seasonal to annual timescales. This reservoir of DOM represents an important source of carbon, energy, and nutrients to marine microbial communities but the identity of the microorganisms and the biochemical pathways underlying the cycling of DOM remain largely uncharacterized. In this study we describe bacteria isolated from the North Pacific Subtropical Gyre (NPSG) near Hawaii that are able to degrade phosphonates associated with high molecular weight dissolved organic matter (HMWDOM), which represents a large fraction of semi-labile DOM. We amended dilution-to-extinction cultures with HMWDOM collected from NPSG surface waters and with purified HMWDOM enriched with polysaccharides bearing alkylphosphonate esters. The HMWDOM-amended cultures were enriched in Roseobacter isolates closely related to Sulfitobacter and close relatives of hydrocarbon-degrading bacteria of the Oceanospirillaceae family, many of which encoded phosphonate degradation pathways. Sulfitobacter cultures encoding C-P lyase were able to catabolize methylphosphonate and 2-hydroxyethylphosphonate, as well as the esters of these phosphonates found in native HMWDOM polysaccharides to acquire phosphorus while producing methane and ethylene, respectively. Conversely, growth of these isolates on HMWDOM polysaccharides as carbon source did not support robust increases in cell yields, suggesting that the constituent carbohydrates in HMWDOM were not readily available to these individual isolates. We postulate that the complete remineralization of HMWDOM polysaccharides requires more complex microbial inter-species interactions. The degradation of phosphonate esters and other common substitutions in marine polysaccharides may be key steps in the turnover of marine DOM. [ABSTRACT FROM AUTHOR]

Dissolved organic matter (DOM) in the oceans is one of the largest pools of reduced carbon on Earth, comparable in size to the atmospheric CO2 reservoir. A vast number of compounds are present in DOM, and they play important roles in all major element cycles, contribute to the storage of atmospheric CO2 in the ocean, support marine ecosystems, and facilitate interactions between organisms. At the heart of the DOM cycle lie molecular-level relationships between the individual compounds in DOM and the members of the ocean microbiome that produce and consume them. In the past, these connections have eluded clear definition because of the sheer numerical complexity of both DOM molecules and microorganisms. Emerging tools in analytical chemistry, microbiology, and informatics are breaking down the barriers to a fuller appreciation of these connections. Here we highlight questions being addressed using recent methodological and technological developments in those fields and consider how these advances are transforming our understanding of some of the most important reactions of the marine carbon cycle. [ABSTRACT FROM AUTHOR]

The role of bacterioplankton in the cycling of marine dissolved organic matter (DOM) is central to the carbon and energy balance in the ocean, yet there are few model organisms available to investigate the genes, metabolic pathways, and biochemical mechanisms involved in the degradation of this globally important carbon pool. To obtain microbial isolates capable of degrading semi-labile DOM for growth, we conducted dilution to extinction cultivation experiments using seawater enriched with high molecular weight (HMW) DOM. In total, 93 isolates were obtained. Amendments using HMW DOM to increase the dissolved organic carbon concentration 4x (280 μM) or 10x (700 μM) the ocean surface water concentrations yielded positive growth in 4-6% of replicate dilutions, whereas <1% scored positive for growth in non-DOM-amended controls. The majority (71%) of isolates displayed a distinct increase in cell yields when grown in increasing concentrations of HMW DOM. Whole-genome sequencing was used to screen the culture collection for purity and to determine the phylogenetic identity of the isolates. Eleven percent of the isolates belonged to the gammaproteobacteria including Alteromonadales (the SAR92 clade) and Vibrio. Surprisingly, 85% of isolates belonged to the methylotrophic OM43 clade of betaproteobacteria, bacteria thought to metabolically specialize in degrading C1 compounds. Growth of these isolates on methanol confirmed their methylotrophic phenotype. Our results indicate that dilution to extinction cultivation enriched with natural sources of organic substrates has a potential to reveal the previously unsuspected relationships between naturally occurring organic nutrients and the microorganisms that consume them. [ABSTRACT FROM AUTHOR]

Marine dissolved organic matter (DOM) contains as much carbon as the Earth's atmosphere, and represents a critical component of the global carbon cycle. To better define microbial processes and activities associated with marine DOM cycling, we analyzed genomic and transcriptional responses of microbial communities to high-molecularweight DOM (HMWDOM) addition. The cell density in the unamended control remained constant, with very few transcript categories exhibiting significant differences over time. In contrast, the DOM-amended microcosm doubled in cell numbers over 27 h, and a variety of HMWDOM-stimulated transcripts from different taxa were observed at all time points measured relative to the control. Transcripts significantly enriched in the HMWDOM treatment included those associated with two-component sensor systems, phosphate and nitrogen assimilation, chemotaxis, and motility. Transcripts from Idiomarina and Alteromonas spp., the most highly represented taxa at the early time points, included those encoding TonB-associated transporters, nitrogen assimilation genes, fatty acid catabolism genes, and TCA cycle enzymes. At the final time point, Methylophaga rRNA and non-rRNA transcripts dominated the HMWDOM-amended microcosm, ahd included gene transcripts associated with both assimilatory and dissimilatory single-carbon compound utilization. The data indicated specific resource partitioning of DOM by different bacterial species, which results in a temporal succession of taxa, metabolic pathways, and chemical transformations associated with HMWDOM turnover. These findings suggest that coordinated, cooperative activities of a variety of bacterial "specialists" may be critical in the cycling of marine DOM, emphasizing the importance of microbial community dynamics in the global carbon cycle. [ABSTRACT FROM AUTHOR]

Abstract: Chemical characterizations of high molecular weight dissolved organic matter (HMW DOM) have shown that a compositionally well-defined family of acylated polysaccharides (APS) contributes a large fraction of DOM in the surface ocean. One process that might affect APS cycling is physical removal by aggregation. To investigate the importance of this mechanism, we compared the chemical composition and transparent exopolymer particle (TEP) abundances of seawater HMW DOM with surface-active organic matter (SAOM) that accumulates as standing sea surface foam during intense wind events. We further simulated the aggregation of SAOM using bubble-adsorption of HMW DOM isolated from laboratory cultures of the diatom Chaetoceros neogracile. 1H-NMR spectroscopy and molecular-level analysis of natural and laboratory-produced HMW DOM and SAOM show important contributions from polysaccharides, acetate, and aliphatic organic matter and similar yields and distributions of neutral sugars after hydrolysis. Microbial degradation of Chaetoceros neogracile DOM removes proteins and mannose-rich polysaccharides to produce HMW DOM with spectral and molecular-level characteristics that resemble seawater APS. These results imply that APS and hydrolysable sugars are resistant to microbial degradation over the time frame of our degradation experiment (40days). As revealed by 1H-NMR spectroscopy and by the neutral monosaccharide data, there are important similarities in the composition of APS in HMW DOM and natural and laboratory-produced SAOM foamy material, rich in TEP. Although these samples are operationally classified in two distinct pools (dissolved vs. particulate) in seawater, they exhibit similar chemical and spectral characteristics. Finally, TEP concentration measurements in SAOM samples indicate that freshly-produced diatom DOM yields SAOM with TEP concentration similar to seawater and natural SAOM, but seven times higher than SAOM produced after bubble-adsorption of degraded HMW DOM. [Copyright &y& Elsevier]

Environmental evidence suggests that Aureococcus anophagefferens (Pelagophyceae), a eukaryotic picoplankton that blooms in coastal seawaters, can outcompete other organisms because of its ability to use abundant dissolved organic nitrogen (DON). To test this hypothesis, we isolated A. anophagefferens in axenic culture and monitored its growth on high-molecular weight (HMW) DON collected from sediment pore waters, a putative source for DON in bays where blooms occur. HMW DON originating from pore water had a substantially higher protein content than surface seawater DON. We found that A. anophagefferens could deplete 25-36% of the available nitrogen in cultures with HMW DON as the sole source of nitrogen and that this corresponded well with the protein fraction in pore-water HMW DON. High rates of cell surface peptide hydrolysis and no detectable N-acetyl polysaccharide hydrolysis, together with the high percentage of hydrolyzable amino acids compared to hydrolyzable aminosugars present in the HMW DON, pointed to the protein fraction as the more likely source of nitrogen used for growth. Whether or not nitrogen scavenging from protein is a common mechanism in phytoplankton is at present unknown but needs to be investigated. [ABSTRACT FROM AUTHOR]

This study focuses on the chemical characterization of high molecular-weight dissolved organic matter (HMW DOM) isolated from the Middle Atlantic Bight in April 1994 and March 1996. Using proton nuclear magnetic resonance spectroscopy (1HNMR) and monosaccharide analysis we compared both spatial and temporal variations in the chemical structure of HMW DOM across this region. Our analyses support the presence of at least two compositionally distinct components to HMW DOM. The major component is acyl polysaccharide (APS), a biopolymer rich in carbohydrates, acetate and lipid, accounting for between 50% and 80% of the total high molecular-weight dissolved organic carbon (HMW DOC) in surface samples. APS is most abundant in fully marine, surface-water samples, and is a product of autochthonous production. Organic matter with spectral properties characteristic of humic substances is the second major component of HMW DOM. Humic substances are most abundant (up to 49% of the total carbon) in samples collected from estuaries, near the coast, and in deep water, suggesting both marine and perhaps terrestrial sources. Radiocarbon analyses of neutral monosaccharides released by the hydrolysis of APS have similar and modern (average 71‰) Δ14C values. Radiocarbon data support our suggestion that these sugars occur as part of a common macromolecule, with an origin via recent biosynthesis. Preliminary radiocarbon data for total neutral monosaccharides isolated from APS at 300 and 750 m show this fraction to be substantially enriched relative to total HMW DOC and DOC. The relatively enriched radiocarbon values of APS at depth suggest APS is rapidly transported into the deep ocean. [Copyright &y& Elsevier]

The southeast subtropical Pacific Ocean was sampled along a zonal transect between the coasts of Chile and Easter Island. This remote area of the world’s ocean presents strong gradients in physical (e.g., temperature, density and light), chemical (e.g., salinity and nutrient concentrations) and microbiological (e.g., cell abundances, biomass and specific growth rates) properties. The goal of this study was to describe the phosphorus (P) dynamics in three main ecosystems along this transect: the upwelling regime off the northern Chilean coast, the oligotrophic area associated with the southeast subtropical Pacific gyre and the transitional area in between these two biomes. We found that inorganic phosphate (Pi) concentrations were high and turnover times were long (>210 nmol l −1 and >31 d, respectively) in the upper water column, along the entire transect. Pi uptake rates in the gyre were low (euphotic layer integrated rates were 0.26 mmol m −2 d −1 in the gyre and 1.28 mmol m −2 d −1 in the upwelling region), yet not only driven by decreases in particle mass or cell abundance (particulate P- and cell- normalized Pi uptake rates in the euphotic layer were ∼1–4 times and ∼3–15 times lower in the gyre than in the upwelling, respectively). However these Pi uptake rates were at or near the maximum Pi uptake velocity (i.e., uptake rates in Pi amended samples were not significantly different from those at ambient concentration: 1.5 and 23.7 nmol l −1 d −1 at 50% PAR in the gyre and upwelling, respectively). Despite the apparent Pi replete conditions, selected dissolved organic P (DOP) compounds were readily hydrolyzed. Nucleotides were the most bioavailable of the DOP substrates tested. Microbes actively assimilated adenosine-5′-triphosphate (ATP) leading to Pi and adenosine incorporation as well as Pi release to the environment. The southeast subtropical Pacific Ocean is a Pi-sufficient environment, yet DOP hydrolytic processes are maintained and contribute to P-cycling across the wide range of environmental conditions present in this ecosystem. [ABSTRACT FROM AUTHOR]

The Mid-Atlantic Bight (MAB) is a highly productive continental shelf region on the eastern North American coast and a potential sight for the export of organic carbon to the open ocean. The dynamics of dissolved organic carbon (DOC) in the MAB were studied during three cruises in April 1994, March 1996 and August 1996 in order to characterize DOC distributions on the shelf, estimate inventories of DOC on the shelf and quantify DOC transport. There were clear spatial and temporal trends in DOC distributions. Concentrations of DOC were greater inshore than offshore and increased southward along the shelf. The total DOC inventory on the shelf during the March and April cruises was estimated at ∼5.88×1012 g C and this increased by 0.4×1012 g C (7%) in August. A simple mass balance of DOC input and export in the MAB resulted in total export of 18.7–19.6×1012g C yr−1. Up to 67% of this carbon is recycled oceanic DOC that is refractory with respect to MAB seawater residence times, ∼4% is introduced through estuaries, sediments and rainwater and at least 29% of the exported shelf DOC (4.1–7.4×1012 g C yr−1) is produced on the shelf. Net ecosystem production of DOC in the MAB is estimated to be between 10% and 18% of MAB primary productivity estimates. Our data supports the hypothesis that the MAB as a whole is net autotrophic for the periods of study and that DOC is an important component in ocean margin carbon budgets. [Copyright &y& Elsevier]

Abstract: We targeted the warm, subsurface waters of the Eastern Mediterranean Sea (EMS) to investigate processes that are linked to the chemical composition and cycling of dissolved organic carbon (DOC) in seawater. The apparent respiration of semi-labile DOC accounted for 27 ± 18% of oxygen consumption in EMS mesopelagic and bathypelagic waters; this value is higher than that observed in the bathypelagic open ocean, so the chemical signals that accompany remineralization of DOC may thus be more pronounced in this region. Ultrafiltered dissolved organic matter (UDOM) collected from four deep basins at depths ranging from 2 to 4350m exhibited bulk chemical (1H-NMR) and molecular level (amino acid and monosaccharide) abundances, composition, and spatial distribution that were similar to previous reports, except for a sample collected in the deep waters of the N. Aegean Sea that had been isolated for over a decade. The amino acid component of UDOM was tightly correlated with apparent oxygen utilization and prokaryotic activity, indicating its relationship with remineralization processes that occur over a large range of timescales. Principal component analyses of relative mole percentages of monomers revealed that oxygen consumption and prokaryotic activity were correlated with variability in amino acid distributions but not well correlated with monosaccharide distributions. Taken together, this study elucidates key relationships between the chemical composition of DOM and heterotrophic metabolism. [Copyright &y& Elsevier]