Transparent exopolymer particles (TEP) in aquatic environments
Introduction
In marine ecosystems, polysaccharides are an important component of the labile fraction of DOC (Benner, Pakulski, McCarthy, Hedges and Hatcher, 1992, Ogawa and Ogura, 1992, Kepkay, Niven and Milligan, 1993, Kepkay, 2000). Because of their high molecular weight they predominantly belong to the colloidal fraction of DOC. Many aquatic organisms, including phytoplankton and bacteria generate large amounts of extracellular polysaccharides (e.g. Hoagland, Rosowski, Gretz and Roemaer, 1993, Costerton, 1995, Myklestad, 1995). Diatoms are especially well known for excreting copious quantities of polysaccharides during all phases of their growth (Watt, 1969, Allan, Lewin and Johnson, 1972, Hellebust, 1974, Hama and Handa, 1983, Sundh, 1989, Williams, 1990). Such exopolymeric substances, called EPS, range in structure from being loose slimes to tight capsules surrounding the cells. One type of EPS, the transparent exopolymer particles (Fig. 1), called TEP, has received increasing attention because the TEP exist as individual particles rather than as cell coatings or dissolved slimes (Alldredge, Passow, & Logan, 1993). The role of TEP in aquatic systems differs from other forms of EPS, because as individual particles not only can they aggregate but also they can be collected by filtration; whereas dissolved substances can only mix with the surrounding water. Although the role of EPS in marine environments has been outlined in several reviews (Hellebust, 1974, Decho, 1990, Leppard, 1995, Myklestad, 1995), our knowledge of TEP has not yet been summarized, and generally these gel particles have been overlooked.
Operationally TEP are defined as transparent particles that are formed from acid polysaccharides and are stainable with alcian blue (Alldredge, Passow & Logan, 1993). Such transparent particles have been noted and described earlier (e.g. Gorden, 1970, Wiebe and Pomeroy, 1972, Emery, Johns and Honjo, 1984) and there have been speculations about their potential importance in marine systems (Smetacek & Pollehne, 1986). However, because techniques for the visualization and quantification of these particles proved elusive, they were largely ignored, but once a method for their visualization was developed their high abundances in marine systems were revealed (Alldredge, Passow & Logan, 1993). How could these TEP have gone largely unnoticed for so long? Their transparency resulted in TEP escaping detection by microscopy, although many microscopists had suspected the presence of such non-visible particles. Other researchers who have spent long hours examining clogged filters have had experience of the effects of their presence. These and other clues, including coagulation theory, had long indicated that additional types of particle were present in seawater, so that the discovery of these elusive, sticky particles at high abundances has not come as a complete surprise.
Once the technique for their visualization of TEP was developed, awareness of the important role played by non-organismal particles in aquatic systems has increased rapidly (e.g. Schumann, Rentsch, Goers, & Schiewer, 2001). Other abundant mucoid particles, the Coomassie Stained Particles (CSP), which are protein-rich, have been discovered (Long & Azam, 1996). In three studies CSP have been found either to be more abundant than TEP (Long & Azam, 1996), or similar in abundance (Grossart, 1999) or less abundant (Prieto, Ruiz, Echevarría, García, Gálvez, Bartual et al., 2002). A careful comparison of both particle types in Lake Kinneret revealed that throughout the year there were, on average, fewer CSP than TEP, possibly because the former have faster turnover rates (Berman & Viner-Mozzini, 2001). The properties of mucoid particles differ in several important aspects from those of solid particles, which consist of organisms and detritus (dead organisms or parts thereof). As mucilage they have properties of gels, e.g. the volume to mass relationship is not constant. As excretion products, the mucoid particles are not subjected to the same constraints of organic C:N:P incorporation as occurs in the production of organic material.
Comparatively little is known about other non-TEP mucoid particles, and so this review will focus on TEP as case examples of mucoid particles, and will summarize the existing knowledge about TEP. Some of the insights gained from studies of TEP will be applicable to the other mucoid particles, but other results appertain more specifically to TEP. The main goal of this summary is to review the role of TEP in different pelagic processes, such as abiotic particle formation, aggregation, sedimentation, food web structure, and carbon cycling and to complement more specific reviews on these topics; e.g. reviews on the production of EPS by microorganisms (Decho, 1990, Myklestad, 1995), on the abiotic formation of particles (Kepkay, 1994), on aggregation (Alldredge and Jackson, 1995, Jackson and Burd, 1998, Thornton, 2002), on microbial ecology (Kirchmann, 2000) and on the role of colloids in carbon cycling (Kepkay, 2000).
The first section of this review describes TEP. After a comparison of methods used to quantify TEP, their global distribution patterns are summarized. Their physico-chemical characteristics will be introduced and their formation discussed. The second section explores their impact on particle dynamics and on the cycling of matter. The effect of the particulate nature of TEP on microorganisms and trace components is speculated upon and the role of TEP for aggregation, particle flux and food web structure is reviewed. The review concludes with a discussion of the role of TEP in the cycling of carbon and on future research goals.
Section snippets
Determination of TEP
TEP are operationally defined as particles retained on polycarbonate filters, which stain with the cationic dye alcian blue. At the pH and concentration used (aqueous solution of 0.02% alcian blue, 8 GX and 0.06% acetic acid, pH of 2.5), this dye stains both sulfated and carboxylated polysaccharides (Passow & Alldredge, 1995b). The particles have to be stained after filteration, as alcian blue precipitates in the presence of salt. Currently there are two methods of measuring TEP, both of which
Abundance and distribution of TEP
The availability of two simple methods to measure TEP has enabled their measurement to be routine, and so providing us with a growing understanding of the role of TEP in aquatic systems. They have been found to be abundant in all waters whether fresh or marine, with concentrations of TEP >5 μm varying between 1 and 8000 ml−1 and concentrations of TEP>2 μm varying between 3000 and 40000 ml−1 (Table 1). Generally, peak concentrations of TEP were associated with phytoplankton blooms (Passow and
Properties of TEP
TEP are a chemically diverse and heterogeneous group of particles. They are exopolymers, but not all exopolymeric substances (EPS) occur as TEP or can form TEP. The precise chemical composition of TEP is unknown, but is known to be highly variable, because the chemical composition of TEP (and their precursors) depend on the species releasing them and the prevailing growth conditions (see below). The physical properties of TEP, such as volume and stability also depend on environmental
Formation of TEP
Dissolved organic matter (DOM), which includes colloids (Koike, Hara, Terauchi and Kogure, 1990, Wells and Goldberg, 1991, Longhurst, Koike, Li, Rodriguez, Dickie, Kepay, Bautista, Ruiz, Wells and Bird, 1992, Wells and Goldberg, 1992) constitutes the largest pool of organic carbon in the ocean and knowledge of the rates and mechanisms by which dissolved organic substances are produced, destroyed, or converted to particulate form is essential if we are to gain a predictive understanding of
Microenvironments of microbes
As particles, TEP contribute structure to the aquatic environment, creating gradients on microscale. Until recently, the environment encountered by aquatic microorganisms was perceived as being largely fluid, relatively homogeneous and governed by diffusive processes. It is now believed that, in fact, aquatic microorganisms live in an environment that is highly structured by the presence of particles that provide physical surfaces, refuge and chemical gradients for microbes (Alldredge and
Cycling of solutes and trace elements
Biogeochemical cycling of elements in marine systems results from complex interactions between dissolved and particulate matter. The cycling of metals, toxins and trace metals depends largely on the presence of polysaccharides, because of the large affinity of dissolved organic substances and trace elements to surface-active exopolymers (Tye, Jepsen, & Lick, 1996). Between 40 and 90% of trace compounds can be scavenged by adsorption onto marine colloids (Buffle, Wilkinson, Stoll, Filella &
Aggregation
The finding that exopolymers can exist as particles has also changed our understanding of the mechanisms promoting aggregation. Aggregation of particles is important for particle dynamics (McCave, 1984) and especially large phytoplankton blooms are frequently terminated by aggregation (Kranck and Milligan, 1988, Alldredge and Gotschalk, 1989). Aggregation theory has been well developed by the colloidal chemistry and aerosol communities and has been applied with varying success to predicting
Flux of particles
The importance of TEP for sedimentation is twofold. Firstly TEP influences the sedimentation of non-TEP particles by aggregating them and secondly TEP themselves contribute directly to the flux of carbon. The fractionation between material that is degraded in the upper ocean and material that sediments to depth depends on the relation between the degradation and the sedimentation rates, so any changes in the average sinking velocity will result in different sedimentation rates. Aggregation
Food-web structure
Which fraction of primary produced particles sinks to depth, also depends on the type of food web present (Rivkin, Legendre, Deibel, Tremblay, Klein, Crocker et al., 1996). Particles may be utilized by bacteria or grazed by eukaryotes. Very little is known about the impact of TEP on the feeding relationships, or on the microbial loop, and the quantitative significance of TEP for these respective pathways can not yet be addressed.
Carbon budget
Although most data on TEP collected to date stems from coastal areas, work in related fields suggests that these gel-like particles exist in all oceanic regions and affect the carbon cycle on global scales.
Conclusions and perspectives
The discovery of the high abundance of colloidal and submicron particles in seawater have changed our understanding of the dynamics of DOM (e.g. Isao, Shigemitsu, Terauchi and Kogure, 1990, Koike, Hara, Terauchi and Kogure, 1990, Wells and Goldberg, 1991, Longhurst, Koike, Li, Rodriguez, Dickie, Kepay, Bautista, Ruiz, Wells and Bird, 1992, Buffle, Filella and Leppard, 1994, Leppard, 1997, Nagata and Kirchmann, 1997). Colloids aggregate like particles (Wells and Goldberg, 1993, Kepkay, 1994),
Acknowledgements
During the last 8 years, countless people have contributed to the work on TEP, and I want to thank them all for adding a small piece to the big puzzle. I enjoyed working with my co-authors and I thank them for a working atmosphere that was fun and productive. Colleagues and reviewers from all over the world have shared their observations, ideas and send encouragement. I especially want to thank Bernt Zeitzschel for his continuous trust and kind nudging of me to write this review, and Alice
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