ReviewAquatic organic matter: Classification and interaction with organic microcontaminants
Graphical abstract
Introduction
Aquatic organic matter is predominantly formed by carbon atoms linked to oxygen, hydrogen, nitrogen, sulfur and other atoms (Stevenson, 1982). These combined elements can be originated either by multiple allochthonous and autochthonous natural sources or anthropogenic inputs (Rocha et al., 2009; Mostofa et al., 2012).
Organic matter (OM) of natural origin is primarily formed by biogeochemical processes such as photosynthesis, excretion of organisms, biomass decay, or diagenesis (Bianchi, 2007). Allochthonous sources consist on leaching the natural OM to aquatic systems via winds, rivers, or groundwater runoff (Jurado et al., 2008; Libes, 2009), which are more relevant to estuarine and coastal regions due to the proximity with sources (Tan, 2014). The gradient distribution of OM along the watercourses from headwaters to rives mouth elicit a series of responses within the structural and functional characteristics of the biological communities, resulting in a continuum of biotic adjustments to adapt to the terrigenous inputs, known as River Continuum Concept (Vannote et al., 1980). In addition, river channels that are characterized by surrounding flood plains, oxbow lakes, mangroves, salt marshes, and seagrass beds may also significantly contribute with allochthonous OM during flooding events (Junk et al., 1989). Autochthonous natural OM is produced in situ (e.g. bacteria, phytoplankton and plants) (Otero et al., 2000; Chester and Jickells, 2012). In the ocean, for instance, most of it is produced by phytoplankton, where other sources are relatively minor (Mostofa et al., 2013). In addition, anthropogenic activities can directly contribute with OM inputs from domestic and industrial sewages, urban runoff, agricultural and forest practices, and industrial organic compounds (Mostofa et al., 2012; Dsikowitzky et al., 2015; Watanabe and Kuwae, 2015; Arruda-Santos et al., 2018). Human activities also may indirectly interfere in OM natural cycles through forest fires (Thomas et al., 2017), river dams (Johnson et al., 1995), among others.
Physically, aquatic OM can be classified in: a) particulate organic matter, which is the fraction retained in a 0.45 μm filter pore (arbitrarily defined); b) dissolved organic matter (DOM), the fraction that passes through this 0.45 μm filter, and; c) colloidal matter organic, with sizes between 1 nm and 1 μm (Mostofa et al., 2012). The sum of DOM and particulate organic matter constitute the total organic matter (Bianchi, 2007; Mostofa et al., 2012). A schematic OM size (μm) and mass (Da) distribution of organisms and chemical species in aquatic system is shown in Fig. 1.
Colloids are particularly interesting since they are included in both dissolved and particulate fractions and, thus, deserve a more detailed discussion. This behavior associated with other characteristics (e.g. Tyndall effect) differ colloid solutions of true solutions (Ranville and Schmiermund, 2002). In aqueous media they are formed by physical and chemical processes (Aboul-Kassim and Simoneit, 2001) and their nature depends of size, shape and surface properties of the particles, as well as particle-particle and particle-solvent interactions (Gustafsson and Gschwend, 1997). According to superficial electrical properties, colloids are considered hydrophilic or hydrophobic. When soluble groups are constituents of the colloidal surface (e.g. fulvic acids (FAc), proteins, and polysaccharides), they promote water affinity (hydrophilic). Otherwise, they will be hydrophobic with neither hydration nor water film formation around the colloid (Gustafsson and Gschwend, 1997; Philippe and Schaumann, 2014). An important characteristic of colloidal dispersion is its large superficial area that favors interaction mechanisms, mobility or sedimentation and cycling of compounds in natural systems (Manahan and Manahan, 2009).
OM cycling influences the global carbon cycle through production, distribution and decomposition of carbon compounds in the biosphere. It may act directly in the cycle of nutrients providing energy, in the form of carbon and nitrogen, to organisms and maintaining the microbial loop (Mostofa et al., 2012; Salonen et al., 2012). OM can also influence the transport, bioavailability and toxicity of organic microcontaminants. However, all these processes depend on the molecules form (e.g. neutral or ionic), aqueous solubility, molecular size and weight, and physicochemical parameters, mainly pH and salinity (Decision et al., 2014). In natural waters, both allochthonous and autochthonous sources of OM are constituted by a complex mixture of non-humic heterogeneous organic substances (NHS), with relatively lower molecular weight (e.g. organics acids, proteins, lipids, carbohydrates, lignin), and humic substances (HS), with variable molecular weight from 500 to >10.000 Da1 (Stevenson, 1982; Otero et al., 2000; Ghabbour and Davies, 2001; Bianchi, 2007).
NHS and HS can be found at any fraction (colloidal, DOM or POM) (Bianchi, 2007). DOM, however, is the most important fraction in aquatic ecosystems since it is involved in a greater number of environmental processes (Søndergaard and Thomas, 2004). Usually, a large fraction of DOM is constituted by HS (~80% of refractory molecules), and about 20% of a labile fraction with well characterized molecular structure (e.g. proteins) (Thoumelin et al., 1997; Chen et al., 2002; Leenheer and Croué, 2003; Gimenes et al., 2010; Arndt et al., 2013). HS are amorphous, heterogeneous and recalcitrant macromolecules originated from incomplete mineralization of organic matter and decay of biomass (Stevenson, 1982). Physicochemical characteristics and composition of HS are variable according to residence time and biogeochemical condition of the environment. This variability generates HS with a wide diversity of elements (number and type) and the presence of several functional groups, resulting in highly reactive molecules (Thoumelin et al., 1997; Gimenes et al., 2010; Arndt et al., 2013).
Due to the complexity of OM sources in aquatic systems, the application of chemical (bio)markers (mainly at the NHS fraction) has been widely used to characterize and differentiate between biogenic and anthropogenic sources (Bianchi and Canuel, 2011). This labile fraction of OM also plays an important role in the aquatic systems, mainly influencing metabolic functions in the organisms, such as enzymatic activities (Lodish et al., 2000; Frimmel et al., 2008). Conversely, studies with HS have focused on their effects on transport, bioavailability and toxicity of environmental contaminants. Many information can be found regarding the interaction between metals (e.g., Wang et al., 2016; Perelomov et al., 2018) and nanocompounds (e.g. Tang et al., 2014) with HS, but limited information is available for the organic microcontaminants despite their growing diversity and potential impacts to the aquatic environment (Meffe and Bustamante, 2014; Fernandez and Gardinali, 2016; Fang et al., 2017).
The organic microcontaminants have more affinity with the refractory fraction of OM (HS fraction mainly). The capacity of binding can be estimated by the partition coefficient of each specific compound to the organic carbon (koc) (De Paolis and Kukkonen, 1997). The main mechanisms of interaction between OM (or HS fraction) and microcontaminants are hydrophobic and electrostatic interactions, sorption process, complexation and hydrogen bond (Gu et al., 1994; Hanrahan, 2010; Rashed, 2013; Orsi, 2014).
The role of HS is already known when related to wastewater treatment (Tang et al., 2014; Sun et al., 2015) and mitigation of metallic and some organic microcontaminants (Tang et al., 2014; Ivanova and Spiteller, 2016; Watanabe et al., 2017). HS may complex with microcontaminants, changing their chemical speciation, and eventually decreasing their toxic potential (Benson and Long, 1991; Arnold et al., 1998; Carlos et al., 2012; Martínez-Zapata et al., 2013). HS significantly affect bioavailability and toxicity since compete with biological tissues for some organic microcontaminants (Leversee et al., 1983). However, these interactions may increase or decrease depending on the class of organic molecule, number and type of binding sites, stability constants, type and concentration of HS (Burgess et al., 2005; Yang et al., 2006; Phyu et al., 2006; Yang et al., 2007; Wiegand et al., 2007; Gourlay-Francé and Tusseau-Vuillemin, 2013). Therefore, to better understand the role of OM (or HS fraction) is essential to know the sources, composition, reactivity and mechanisms of mediating action with the contaminants (Perminova et al., 2006).
In this context, the present review focuses on the main groups that constitute the NHS (carbohydrates, proteins, lipids, and lignin) and their role as chemical biomarkers, as well as the main characteristics of HS are presented focusing on their functions, properties and mechanisms specifically associated to bioavailability, transport and toxicity of organic microcontaminants.
Section snippets
Non-humic substances (NHS)
NHS are labile compounds constituted by a complex mixture of elements formed by covalent bonds. They can be grouped into classes based on similarities of their functional groups and metabolic functions in the organisms (Libes, 2009). The most important classes are carbohydrates, proteins, lipids, and lignins that are the most easily synthesized biopolymers, susceptible to assimilation by biota, and degradation by microorganisms (Stevenson, 1982; Killops and Killops, 2013).
NHS perform a key role
Humic substances
Unlike NHS, HS do not have several classes of compounds and, therefore, are presented according to their physicochemical characteristics and solubility in aqueous medium. Thurman (1985), for instance, defined HS based on chromatographic extraction methods (XAD ion exchange resin), isolating them from the aquatic environmental. HS are a non–specific portion, polyelectrolyte and polar organic acid macromolecules. According to Stevenson (1982), HS are yellow to brown color substances with
Considerations and recommendations
Knowledge about OM has substantially increased in the last decades, especially regarding identification of sources, elemental composition, seasonal influence, as well as pH and salinity effects upon production, distribution, speciation, and environmental levels of OM. Chemical composition of NHS is well elucidated and protein, lipids and others biopolymers are used as reliable tools for identifying natural and anthropogenic OM sources in aquatic environment. On the other hand, although advances
Acknowledgments
The research was funded by FINEP (Project No 01.11.0038.0 and 01.14.0141.00). G Fillmann is a research fellow of the Brazilian Research Council (CNPq PQ 312341/2013-0). V. Artifon was sponsored by CNPq (PhD grant No 1384392).
References (274)
- et al.
Trihalomethane formation potential of aquatic and terrestrial fulvic and humic acids: sorption on activated carbon
Sci. Total Environ.
(2015) - et al.
Bioavailability of atrazine, pyrene and benzo[a]pyrene in European river waters
Chemosphere
(2001) - et al.
Sterols as biomarkers in the surface microlayer of the estuarine areas
Mar. Pollut. Bull.
(2015) - et al.
Identification of proteomic signatures of exposure to marine pollutants in mussels (Mytilus edulis)
Mol. Cell. Proteomics
(2006) - et al.
Quantifying the degradation of organic matter in marine sediments: a review and synthesis
Earth Sci. Rev.
(2013) - et al.
Sources and distribution of aromatic hydrocarbons in a tropical marine protected area estuary under influence of sugarcane cultivation
Sci. Total Environ.
(2018) - et al.
Influence of natural dissolved organic matter (DOM) on acute and chronic toxicity of the pesticides chlorothalonil, chlorpyrifos and fipronil on the benthic estuarine copepod Amphiascus tenuiremis
J. Exp. Mar. Biol. Ecol.
(2005) - et al.
Evaluation of humic-pesticide interactions on the acute toxicity of selected organophosphate and carbamate insecticides
Ecotoxicol. Environ. Saf.
(1991) - et al.
Particulate organic carbon cycling and transformation
- et al.
Dissolved and particulate carbohydrates in contrasting marine sediments
Geochim. Cosmochim. Acta
(2000)
Lipids as biomarkers for carbon cycling on the Northwest Shelf of Australia: results from a sediment trap study
Mar. Chem.
A surface tension based method for measuring oil dispersant concentration in seawater
Mar. Pollut. Bull.
Proteomic research in bivalves
J. Proteome
Photochemical fate of a mixture of emerging pollutants in the presence of humic substances
Water Res.
Sterols as markers of sewage contamination in a tropical urban estuary (Guanabara Bay, Brazil): space–time variations
Estuar. Coast. Shelf Sci.
Lipids in the sedimentary record as markers of the sources and deposition of organic matter in a tropical Brazilian estuarine–lagoon system
Mar. Chem.
Distribution and characterization of organic matter using lipid biomarkers: a case study in a pristine tropical bay in NE Brazil
Estuar. Coast. Shelf Sci.
Urban sewage lipids in the suspended particulate matter of a coral reef under river influence in the South West Gulf of Mexico
Water Res.
Spectroscopic characterization of the structural and functional properties of natural organic matter fractions
Chemosphere
Polycyclic aromatic hydrocarbon (PAH) distributions and associations with organic matter in surface waters of the York River, VA Estuary
Org. Geochem.
Binding of organic pollutants to humic and fulvic acids: influence of pH and the structure of humic material
Chemosphere
Lipid biomarkers and spectroscopic indices for identifying organic matter sources in aquatic environments: a review
Water Res.
Spatiotemporal variations in the abundance and composition of bulk and chromophoric dissolved organic matter in seasonally hypoxia-influenced Green Bay, Lake Michigan, USA
Sci. Total Environ.
Identification of characteristic organic contaminants in wastewaters from modern paper production sites and subsequent tracing in a river
J. Hazard. Mater.
Distribution and sources of n-alkanes and polycyclic aromatic hydrocarbons in shellfish of the Egyptian Red Sea coast
Egypt. J. Aquat. Res.
Source characterization of sedimentary organic matter using molecular and stable carbon isotopic composition of n-alkanes and fatty acids in sediment core from Lake Dianchi, China
Sci. Total Environ.
Bioaccumulation and bioavailability of tributyltin chloride: influence of pH and humic acids
Water Res.
Emerging roles for conjugated sterols in plants
Prog. Lipid Res.
An n-alkane proxy for the sedimentary input of submerged/floating freshwater aquatic macrophytes
Org. Geochem.
Fatty acid profiling as bioindicator of chemical stress in marine organisms: a review
Ecol. Indic.
Spatial and temporal distribution of chromophoric dissolved organic matter (CDOM) fluorescence and its contribution to light attenuation in UK waterbodies
Estuar. Coast. Shelf Sci.
Quantitative modeling of bioconcentration factors of carbonyl herbicides using multivariate image analysis
Chemosphere
Photochemical generation and decay kinetics of superoxide and hydrogen peroxide in the presence of standard humic and fulvic acids
Water Res.
Predicting the bioconcentration factor of highly hydrophobic organic chemicals
Food Chem. Toxicol.
Aqueous photochemical degradation of hydroxylated PAHs: kinetics, pathways, and multivariate effects of main water constituents
Sci. Total Environ.
Amelioration of the photo-induced toxicity of polycyclic aromatic hydrocarbons by a commercial humic acid
Ecotoxicol. Environ. Saf.
Expert QSAR system for predicting the bioconcentration factor under the REACH regulation
Environ. Res.
Carbohydrates as ligands: coordination equilibria and structure of the metal complexes
Coord. Chem. Rev.
Lipid biomarker stratigraphic records through the Late Devonian Frasnian/Famennian boundary: comparison of high and low latitude epicontinental marine settings
Org. Geochem.
Effects of dissolved organic matter (DOM) on the bioconcentration of organic chemicals in aquatic organisms - a review
Chemosphere
Interaction mechanisms between organic pollutants and solid phase systems
Measuring the bioavailability of two hydrophobic organic compounds in the presence of dissolved organic matter
Environ. Toxicol. Chem.
Photo-induced toxicity of deepwater horizon slick oil to blue crab (Callinectes sapidus) larvae
Environ. Toxicol. Chem.
Association of triorganotin compounds with dissolved humic acids
Environ. Sci. Technol.
A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms
Environ. Rev.
Lipids in Aquatic Ecosystems
A review and comparison of models for predicting dynamic chemical bioconcentration in fish
Environ. Toxicol. Chem.
Photoenhanced toxicity of petroleum to aquatic invertebrates and fish
Arch. Environ. Contam. Toxicol.
Quantification of sterol and triterpenol biomarkers in sediments of the Cananéia-Iguape estuarine-lagoonal system (Brazil) by UHPLC-MS/MS
Int. J. Anal. Chem.
Biogeochemistry of Estuaries
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