Dissolved organic carbon

Dissolved organic carbon (DOC) is the fraction of organic carbon operationally defined as that which can pass through a filter with a pore size typically between 0.22 and 0.7 micrometers.[2] The fraction remaining on the filter is called particulate organic carbon (POC).[3]

Net ocean DOC production and export fluxes
Net DOC production (NDP) in the upper 74 metres (a) and net DOC export (NDX) below 74 metres (b). At steady state, the global summation of NDX is equal to that of NDP, and is 2.31 ± 0.60 PgC yr.[1]

Dissolved organic matter (DOM) is a closely related term often used interchangeably with DOC. While DOC refers specifically to the mass of carbon in the dissolved organic material, DOM refers to the total mass of the dissolved organic matter. So DOM also includes the mass of other elements present in the organic material, such as nitrogen, oxygen and hydrogen. DOC is a component of DOM and there is typically about twice as much DOM as DOC.[4] Many statements that can be made about DOC apply equally to DOM, and vice versa.

DOC is abundant in marine and freshwater systems and is one of the greatest cycled reservoirs of organic matter on Earth, accounting for the same amount of carbon as in the atmosphere and up to 20% of all organic carbon.[5] In general, organic carbon compounds are the result of decomposition processes from dead organic matter including plants and animals. DOC can originate from within or outside any given body of water. DOC originating from within the body of water is known as autochthonous DOC and typically comes from aquatic plants or algae, while DOC originating outside the body of water is known as allochthonous DOC and typically comes from soils or terrestrial plants.[6] When water originates from land areas with a high proportion of organic soils, these components can drain into rivers and lakes as DOC.

The marine DOC pool is important for the functioning of marine ecosystems because they are at the interface between the chemical and the biological worlds. DOC fuels marine food webs, and is a major component of the Earth’s carbon cycling.[7]

Overview

Size and classification of marine particles[8]
Adapted from Simon et al., 2002.[9]
Colour differences in DOC collected from coastal waters
Filtered (0.2 μm) coastal marine waters collected at various locations around the United Kingdom. The differences in colour is due to the range of soil-derived carbon input to the coastal water, with dark brown (left) indicating a high soil-derived carbon contribution and near-clear water (right) indicating a low soil-derived carbon contribution.[7]

DOC is a basic nutrient, supporting growth of microorganisms and plays an important role in the global carbon cycle through the microbial loop.[10] In some organisms (stages) that do not feed in the traditional sense, dissolved matter may be the only external food source.[11] Moreover, DOC is an indicator of organic loadings in streams, as well as supporting terrestrial processing (e.g., within soil, forests, and wetlands) of organic matter. Dissolved organic carbon has a high proportion of biodegradable dissolved organic carbon (BDOC) in first order streams compared to higher order streams. In the absence of extensive wetlands, bogs, or swamps, baseflow concentrations of DOC in undisturbed watersheds generally range from approximately 1 to 20 mg/L carbon.[12] Carbon concentrations considerably vary across ecosystems. For example, the Everglades may be near the top of the range and the middle of oceans may be near the bottom. Occasionally, high concentrations of organic carbon indicate anthropogenic influences, but most DOC originates naturally.[13]

The BDOC fraction consists of organic molecules that heterotrophic bacteria can use as a source of energy and carbon. [14] Some subset of DOC constitutes the precursors of disinfection byproducts for drinking water.[15] BDOC can contribute to undesirable biological regrowth within water distribution systems.[16]

The dissolved fraction of total organic carbon (TOC) is an operational classification. Many researchers use the term "dissolved" for compounds that pass through a 0.45 μm filter, but 0.22 μm filters have also been used to remove higher colloidal concentrations.

A practical definition of dissolved typically used in marine chemistry is all substances that pass through a GF/F filter, which has a nominal pore size of approximately 0.7 μm (Whatman glass microfiber filter, 0.6–0.8 μm particle retention[17]). The recommended procedure is the HTCO technique, which calls for filtration through pre-combusted glass fiber filters, typically the GF/F classification.[18]

Labile and recalcitrant

Dissolved organic matter can be classified as labile or as recalcitrant, depending on its reactivity. Recalcitrant DOC is also called refractory DOC, and these terms seem to be used interchangeably in the context of DOC. Depending on the origin and composition of DOC, its behavior and cycling are different; the labile fraction of DOC decomposes rapidly through microbially or photochemically mediated processes, whereas refractory DOC is resistant to degradation and can persist in the ocean for millennia. In the coastal ocean, organic matter from terrestrial plant litter or soils appears to be more refractory[19] and thus often behaves conservatively. In addition, refractory DOC is produced in the ocean by the bacterial transformation of labile DOC, which reshapes its composition.[20][21][22]

Due to the continuous production and degradation in natural systems, the DOC pool contains a spectrum of reactive compounds each with their own reactivity,[23] that have been divided into fractions from labile to recalcitrant, depending on the turnover times,[24] as shown in the following table...

DOC pool spectrum from labile to recalcitrant [23][24]
DOC fraction acronym turnover time amount
labile DOCL hours to days < 200 Tg C
semi-labile DOCSL weeks to months ∼600 Tg C
semi-recalcitrant DOCSR decades ∼1400 Tg C
recalcitrant DOCR thousands of years ∼63000 Tg C
highly resistant tens of thousands of years

This wide range in turnover or degradation times has been linked with the chemical composition, structure and molecular size,[25][26] but degradation also depends on the environmental conditions (e.g., nutrients), prokaryote diversity, redox state, iron availability, mineral-particle associations, temperature, sun-light exposure, biological production of recalcitrant compounds, and the effect of priming or dilution of individual molecules.[25][27][28][29][30][31] For example, lignin can be degraded in aerobic soils but is relatively recalcitrant in anoxic marine sediments.[32] This example shows bioavailability varies as a function of the ecosystem’s properties. Accordingly, even normally ancient and recalcitrant compounds, such as petroleum, carboxyl-rich alicyclic molecules, can be degraded in the appropriate environmental setting.[33][34]

Terrestrial ecosystems

Soil

Soil DOC sources and sinks [35]
Sources and sinks of dissolved organic carbon in the soil system
Groundwater DOC sources
Origins and bioavailability of DOC in groundwater [36]
DOM: dissolved organic matter
Freshwater DOC sources and sinks [37]
DOC and POC — DIC and PIC
Inland waters primarily receive carbon from terrestrial ecosystems.[38] This carbon (1.9 Pg C y-1) is transported to the oceans (0.9 Pg C y-1), buried in the sediments (0.2 Pg C y-1) or emitted as CO2 (0.8 Pg C y-1).[39] More recent estimations are different: In 2013, Raymond et al. claimed CO2 emission from inland waters can be as high as 2.1 Pg C y-1.[40]
                   P = photosynthesis                    R = respiration

Dissolved organic matter (DOM) is one of the most active and mobile carbon pools and has an important role in global carbon cycling.[41] In addition, dissolved organic carbon (DOC) affects the soil negative electrical charges denitrification process, acid-base reactions in the soil solution, retention and translocation of nutrients (cations), and immobilization of heavy metals and xenobiotics.[42] Soil DOM can be derived from different sources (inputs), such as atmospheric carbon dissolved in rainfall, litter and crop residues, manure, root exudates, and decomposition of soil organic matter (SOM). In the soil, DOM availability depends on its interactions with mineral components (e.g., clays, Fe and Al oxides) modulated by adsorption and desorption processes.[43] It also depends on SOM fractions (e.g., stabilized organic molecules and microbial biomass) by mineralization and immobilization processes. In addition, the intensity of these interactions changes according to soil inherent properties,[44] land use, and crop management.[43][35]

During the decomposition of organic material, most carbon is lost as CO2 to the atmosphere by microbial oxidation. Soil type and landscape slope, leaching, and runoff are also important processes associated to DOM losses in the soil.[45] In well-drained soils, leached DOC can reach the water table and release nutrients and pollutants that can contaminate groundwater,[46][47] whereas runoff transports DOM and xenobiotics to other areas, rivers, and lakes.[35]

Groundwater

Precipitation and surface water leaches dissolved organic carbon (DOC) from vegetation and plant litter and percolates through the soil column to the saturated zone. The concentration, composition, and bioavailability of DOC are altered during transport through the soil column by various physicochemical and biological processes, including sorption, desorption, biodegradation and biosynthesis. Hydrophobic molecules are preferentially partitioned onto soil minerals and have a longer retention time in soils than hydrophilic molecules. The hydrophobicity and retention time of colloids and dissolved molecules in soils are controlled by their size, polarity, charge, and bioavailability. Bioavailable DOM is subjected to microbial decomposition, resulting in a reduction in size and molecular weight. Novel molecules are synthesized by soil microbes, and some of these metabolites enter the DOC reservoir in groundwater.[36]

Freshwater ecosystems

Aquatic carbon occurs in different forms. Firstly, a division is made between organic and inorganic carbon. Organic carbon is a mixture of organic compounds originating from detritus or primary producers. It can be divided into POC (particulate organic carbon; particles > 0.45 μm) and DOC (dissolved organic carbon; particles < 0.45 μm). DOC usually makes up 90% of the total amount of aquatic organic carbon. Its concentration ranges from 0.1 to >300 mg L-1.[48]

Likewise, inorganic carbon also consists of a particulate (PIC) and a dissolved phase (DIC). PIC mainly consists of carbonates (e.g., CaCO3), DIC consists of carbonate (CO32-), bicarbonate (HCO3-), CO2 and a negligibly small fraction of carbonic acid (H2CO3). The inorganic carbon compounds exist in equilibrium that depends on the pH of the water.[49] DIC concentrations in freshwater range from about zero in acidic waters to 60 mg C L-1 in areas with carbonate-rich sediments.[50]

POC can be degraded to form DOC; DOC can become POC by flocculation. Inorganic and organic carbon are linked through aquatic organisms. CO2 is used in photosynthesis (P) by for instance macrophytes, produced by respiration (R), and exchanged with the atmosphere. Organic carbon is produced by organisms and is released during and after their life; e.g., in rivers, 1–20% of the total amount of DOC is produced by macrophytes.[38] Carbon can enter the system from the catchment and is transported to the oceans by rivers and streams. There is also exchange with carbon in the sediments, e.g., burial of organic carbon, which is important for carbon sequestration in aquatic habitats.[51]

Aquatic systems are very important in global carbon sequestration; e.g., when different European ecosystems are compared, inland aquatic systems form the second largest carbon sink (19–41 Tg C y-1); only forests take up more carbon (125–223 Tg C y-1).[52][37]

Marine ecosystems

Ocean DOC sources and sinks [7]
Simplified view of the main sources (black text; underlined are the allochthonous sources) and sinks (yellow text) of the oceanic dissolved organic carbon (DOC) pool.
Main sources
Most commonly referred sources of DOC are: atmospheric (e.g., rain and dust), terrestrial (e.g., rivers), primary producers (e.g., microalgae, cyanobacteria, macrophytes), groundwater, food chain processes (e.g., zooplankton grazing), and benthic fluxes (exchange of DOC across the sediment-water interface but also from hydrothermal vents).[7]
Main sinks
The four main processes removing DOC from the water column are: photodegradation (particularly UV-radiation – though sometimes photodegradation "transforms" DOC rather than removing it, ending up with higher molecular weight complex molecules), microbial (mainly by prokaryotes), aggregation (primarily when river and seawater mixes) and thermal degradation (in e.g., hydrothermal systems).[7]

Sources

In marine systems DOC originates from either autochthonous or allochthonous sources. Autochthonous DOC is produced within the system, primarily by plankton organisms [53][54] and in coastal waters additionally by benthic microalgae, benthic fluxes, and macrophytes,[55] whereas allochthonous DOC is mainly of terrestrial origin supplemented by groundwater and atmospheric inputs.[56][57] In addition to soil derived humic substances, terrestrial DOC also includes material leached from plants exported during rain events, emissions of plant materials to the atmosphere and deposition in aquatic environments (e.g., volatile organic carbon and pollens), and also thousands of synthetic human-made organic chemicals that can be measured in the ocean at trace concentrations.[58][59][7]

Phytoplankton

Phytoplankton produces DOC by extracellular release commonly accounting between 5 and 30% of their total primary production,[60] although this varies from species to species.[61] Nonetheless, this release of extracellular DOC is enhanced under high light and low nutrient levels, and thus should increase relatively from eutrophic to oligotrophic areas, probably as a mechanism for dissipating cellular energy.[62] Phytoplankton can also produce DOC by autolysis during physiological stress situations e.g., nutrient limitation.[63] Other studies have demonstrated DOC production in association with meso- and macro-zooplankton feeding on phytoplankton and bacteria.[64][7]

Zooplankton

Zooplankton-mediated release of DOC occurs through sloppy feeding, excretion and defecation which can be important energy sources for microbes.[65][64] Such DOC production is largest during periods with high food concentration and dominance of large zooplankton species.[66][7]

Bacteria and viruses

Bacteria are often viewed as the main consumers of DOC, but they can also produce DOC during cell division and viral lysis.[67][68][69] The biochemical components of bacteria are largely the same as other organisms, but some compounds from the cell wall are unique and are used to trace bacterial derived DOC (e.g., peptidoglycan). These compounds are widely distributed in the ocean, suggesting that bacterial DOC production could be important in marine systems.[70] Viruses are the most abundant life forms in the oceans infecting all life forms including algae, bacteria and zooplankton.[71] After infection, the virus either enters a dormant (lysogenic) or productive (lytic) state.[72] The lytic cycle causes disruption of the cell(s) and release of DOC.[73][7]

Simplified microbial food web in the sunlit ocean
Left side: classic description of the carbon flow from photosynthetic algae to grazers and higher trophic levels in the food chain.
Right side: microbial loop, with bacteria using dissolved organic carbon to gain biomass, which then re-enters the classic carbon flow through protists.[74][75]
Dissolved organic carbon (DOC) fluxes in the surface, mesopelagic, and interior ocean
In panel (A) oceanic DOC stocks are shown in black circles with red font and units are Pg-C. DOC fluxes are shown in black and white font and units are either Tg-C yr–1 or Pg-C yr–1. Letters in arrows and associated flux values correspond to descriptions displayed in (B), which lists sources and sinks of oceanic DOC.[76]

Macrophytes

Marine macrophytes (i.e., macroalgae and seagrass) are highly productive and extend over large areas in coastal waters but their production of DOC has not received much attention. Macrophytes release DOC during growth with a conservative estimate (excluding release from decaying tissues) suggesting that macroalgae release between 1-39% of their gross primary production,[77][78] while seagrasses release less than 5% as DOC of their gross primary production.[79] The released DOC has been shown to be rich in carbohydrates, with rates depending on temperature and light availability.[80][81] Globally the macrophyte communities have been suggested to produce ∼160 Tg C yr–1 of DOC, which is approximately half the annual global river DOC input (250 Tg C yr–1).[80][7]

Marine sediments

Peatland river water draining into coastal waters
South-East Asia is home to one of the world's largest stores of tropical peatland and accounts for roughly 10 % of the global land-to-sea dissolved organic carbon (DOC) flux. The rivers carry high coloured dissolved organic matter (CDOM) concentrations, shown here interfacing with ocean shelf water.[82]

Marine sediments represent the main sites of OM degradation and burial in the ocean, hosting microbes in densities up to 1000 times higher than found in the water column.[83] The DOC concentrations in sediments are often an order of magnitude higher than in the overlying water column.[84] This concentration difference results in a continued diffusive flux and suggests that sediments are a major DOC source releasing 350 Tg C yr–1, which is comparable to the input of DOC from rivers.[85] This estimate is based on calculated diffusive fluxes and does not include resuspension events which also releases DOC [86] and therefore the estimate could be conservative. Also, some studies have shown that geothermal systems and petroleum seepage contribute with pre-aged DOC to the deep ocean basins,[87][88] but consistent global estimates of the overall input are currently lacking. Globally, groundwaters account for an unknown part of the freshwater DOC flux to the oceans.[89] The DOC in groundwater is a mixture of terrestrial, infiltrated marine, and in situ microbially produced material.[90] This flux of DOC to coastal waters could be important, as concentrations in groundwater are generally higher than in coastal seawater,[91] but reliable global estimates are also currently lacking.[7]

Sinks

The main processes that remove DOC from the ocean water column are: (1) Thermal degradation in e.g., submarine hydrothermal systems;[92] (2) bubble coagulation and abiotic flocculation into microparticles [93] or sorption to particles;[94] (3) abiotic degradation via photochemical reactions;[95][96] and (4) biotic degradation by heterotrophic marine prokaryotes.[97] It has been suggested that the combined effects of photochemical and microbial degradation represent the major sinks of DOC.[98][7]

Thermal degradation

Thermal degradation of DOC has been found at high-temperature hydrothermal ridge-flanks, where outflow DOC concentrations are lower than in the inflow. While the global impact of these processes has not been investigated, current data suggest it is a minor DOC sink.[100] Abiotic DOC flocculation is often observed during rapid (minutes) shifts in salinity when fresh and marine waters mix.[101] Flocculation changes the DOC chemical composition, by removing humic compounds and reducing molecular size, transforming DOC to particulate organic flocs which can sediment and/or be consumed by grazers and filter feeders, but it also stimulates the bacterial degradation of the flocculated DOC.[102] The impacts of flocculation on the removal of DOC from coastal waters are highly variable with some studies suggesting it can remove up to 30% of the DOC pool,[103][104] while others find much lower values (3–6%;[105]). Such differences could be explained by seasonal and system differences in the DOC chemical composition, pH, metallic cation concentration, microbial reactivity, and ionic strength.[101][106][7]

CDOM

The colored fraction of DOC (CDOM) absorbs light in the blue and UV-light range and therefore influences plankton productivity both negatively by absorbing light, that otherwise would be available for photosynthesis, and positively by protecting plankton organisms from harmful UV-light.[107][108] However, as the impact of UV damage and ability to repair is extremely variable, there is no consensus on how UV-light changes might impact overall plankton communities.[109][110] The CDOM absorption of light initiates a complex range of photochemical processes, which can impact nutrient, trace metal and DOC chemical composition, and promote DOC degradation.[111]

Photodegradation

Photodegradation involves the transformation of CDOM into smaller and less colored molecules (e.g., organic acids), or into inorganic carbon (CO, CO2), and nutrient salts (NH+4, HPO2−4).[112][113][114] Therefore, it generally means that photodegradation transforms recalcitrant into labile DOC molecules that can be rapidly used by prokaryotes for biomass production and respiration. However, it can also increase CDOM through the transformation of compounds such as triglycerides, into more complex aromatic compounds,[115][116] which are less degradable by microbes. Moreover, UV radiation can produce e.g., reactive oxygen species, which are harmful to microbes.[117] The impact of photochemical processes on the DOC pool depends also on the chemical composition,[118] with some studies suggesting that recently produced autochthonous DOC becomes less bioavailable while allochthonous DOC becomes more bioavailable to prokaryotes after sunlight exposure, albeit others have found the contrary.[119][120][121] Photochemical reactions are particularly important in coastal waters which receive high loads of terrestrial derived CDOM, with an estimated ∼20–30% of terrestrial DOC being rapidly photodegraded and consumed.[122] Global estimates also suggests that in marine systems photodegradation of DOC produces ∼180 Tg C yr–1 of inorganic carbon, with an additional 100 Tg C yr–1 of DOC made more available to microbial degradation.[123][124] Another attempt at global ocean estimates also suggest that photodegradation (210 Tg C yr–1) is approximately the same as the annual global input of riverine DOC (250 Tg C yr–1;[125]), while others suggest that direct photodegradation exceeds the riverine DOC inputs.[126][127][7]

Recalcitrant DOC

Change in the composition of DOC with depth

Distribution

More precise measurement techniques developed in the late 1990s have allowed for a good understanding of how dissolved organic carbon is distributed in marine environments both vertically and across the surface.[128] It is now understood that dissolved organic carbon in the ocean spans a range from very labile to very recalcitrant (refractory). The labile dissolved organic carbon is mainly produced by marine organisms and is consumed in the surface ocean, and consists of sugars, proteins, and other compounds that are easily used by marine bacteria.[129] The recalcitrant dissolved organic carbon is evenly spread throughout the water column and consists of high molecular weight and structurally complex compounds that are difficult for marine organisms to use such as the lignin, pollen, or humic acids.[130] Therefore, the observed vertical distribution consists of high concentrations of labile DOC in the upper water column and low concentrations at depth.

In addition to vertical distributions, horizontal distributions have been modeled and sampled as well.[131] In the surface ocean at a depth of 30 meters, the higher dissolved organic carbon concentrations are found in the South Pacific Gyre, the South Atlantic Gyre, and the Indian Ocean. At a depth of 3,000 meters, highest concentrations are in the North Atlantic Deep Water where dissolved organic carbon from the high concentration surface ocean is removed to depth. While in the northern Indian Ocean high DOC is observed due to high fresh water flux and sediments. Since the time scales of horizontal motion along the ocean bottom are in the thousands of years, the refractory dissolved organic carbon is slowly consumed on its way from the North Atlantic and reaches a minimum in the North Pacific.

As emergent

Dissolved organic matter is a heterogeneous pool of thousands, likely millions, of organic compounds. These compounds differ not only in composition and concentration (from pM to μM), but also originate from various organisms (phytoplankton, zooplankton, and bacteria) and environments (terrestrial vegetation and soils, coastal fringe ecosystems) and may have been produced recently or thousands of years ago. Moreover, even organic compounds deriving from the same source and of the same age may have been subjected to different processing histories prior to accumulating within the same pool of DOM.[76]

Interior ocean DOM is a highly modified fraction that remains after years of exposure to sunlight, utilization by heterotrophs, flocculation and coagulation, and interaction with particles. Many of these processes within the DOM pool are compound- or class-specific. For example, condensed aromatic compounds are highly photosensitive,[132] whereas proteins, carbohydrates, and their monomers are readily taken up by bacteria.[133][134][135] Microbes and other consumers are selective in the type of DOM they utilize and typically prefer certain organic compounds over others. Consequently, DOM becomes less reactive as it is continually reworked. Said another way, the DOM pool becomes less labile and more refractory with degradation. As it is reworked, organic compounds are continually being added to the bulk DOM pool by physical mixing, exchange with particles, and/or production of organic molecules by the consumer community.[136][137][138][139] As such, the compositional changes that occur during degradation are more complex than the simple removal of more labile components and resultant accumulation of remaining, less labile compounds.[76]

Dissolved organic matter recalcitrance (i.e., its overall reactivity toward degradation and/or utilization) is therefore an emergent property. The perception of DOM recalcitrance changes during organic matter degradation and in conjunction with any other process that removes or adds organic compounds to the DOM pool under consideration.[76]

Interaction with metals

DOC also facilitates the transport of metals in aquatic systems. Metals form complexes with DOC, enhancing metal solubility while also reducing metal bioavailability.

DOM isolation and analysis

DOM is found in low concentrations in nature for direct analysis with NMR or MS. Moreover, DOM samples often contain high concentrations of inorganic salts that are incompatible with such techniques.[140] Therefore, it is necessary a concentration and isolation step of the sample.[141][142] The most used isolation techniques are ultrafiltration, reverse osmosis and solid-phase extraction.[143] Among them solid-phase extraction is considered as the cheapest and easiest technique[144]

See also

References

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