Elsevier

Science of The Total Environment

Volume 649, 1 February 2019, Pages 1620-1635
Science of The Total Environment

Review
Aquatic organic matter: Classification and interaction with organic microcontaminants

https://doi.org/10.1016/j.scitotenv.2018.08.385Get rights and content

Highlights

  • Systematic classification of OM according to sources, size and type

  • Relative importance of different kinds of OM

  • Relevance of OM compounds as molecular markers

  • Role of OM upon organic microcontaminants within aquatic ecosystems

  • Unique experimental protocols hinder data comparison

Abstract

Organic matter (OM) in aquatic system is originated from autochthonous and allochthonous natural sources as well as anthropogenic inputs, and can be found in dissolved, particulate or colloidal form. According to the type/composition, OM can be divided in non-humic substances (NHS) or humic substances (HS). 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. HS functions, properties and mechanisms are discussed, in addition to their association to the fate, bioavailability, and toxicity of organic microcontaminants in the aquatic systems. Despite the growing diversity and potential impacts of organic microcontaminants to the aquatic environment, limited information is available about their association with OM. A protective effect is, however, normally seen since the presence of OM (HS mainly) may reduce bioavailability and, consequently, the concentration of organic microcontaminants within the organism. It may also affect the toxicity by either absorbing ultraviolet radiation incidence and, then, reducing the formation of phototoxic compounds, or by increasing the oxygen reactive species and, thus, affecting the decomposition of natural and anthropogenic organic compounds. In addition, the outcome data is hard to compare since each study follows unique experimental protocols. The often use of commercial humic acid (Aldrich) as a generic source of OM in studies can also hinder comparisons since differences in composition makes this type of OM not representative of any aquatic environment. Thus, the current challenge is find out how this clear fragmentation can be overcome.

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).

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