WATER QUALITY: Technical Information--Briefing paper on "The ecological role(s) of aquatic microorganisms in lakes and reservoirs" In Reply Refer To: August 26, 1980 EGS-Mail Stop 412 QUALITY OF WATER BRANCH TECHNICAL MEMORANDUM NO. 80.23 Subject: WATER QUALITY: Technical Information--Briefing paper on "The ecological role(s) of aquatic microorganisms in lakes and reservoirs" by Bruce L. Kimmel, Biological Station and Department of Zoology, University of Oklahoma, Norman, Oklahoma The enclosed discussion of "The ecological role(s) of aquatic microorganisms in lakes and reservoirs" was prepared at the request of the Quality of Water Branch by Dr. Bruce Kimmel, Assistant Director, University of Oklahoma Biological Station. Bruce has been extremely helpful in assisting with our training course "Fundamentals of Lake Limnology" which is held at the Biological Station. This briefing paper is a continuation of the series initiated by the Quality of Water Branch in August, 1974. Please circulate it as widely as possible in all District and project offices. R. J. Pickering Chief, Quality of Water Branch Enclosure Key words: water quality, information, briefing paper, microorganisms, bacteria. Superceded memoranda: none WRD Distribution: A, B, FO-L, PO THE ECOLOGICAL ROLE(S) OF AQUATIC MICROORGANISMS IN LAKES AND RESERVOIRS by Bruce L. Kimmel 1/ ABSTRACT Microorganisms form vital links in the structure of aquatic ecosystems by virtue of their roles in organic matter production and decomposition, nutrient uptake and regeneration, foodweb transfers, and biogeochemical transformations. By the nature of their biological activities, autotrophic and heterotrophic microorganisms are sensitive indicators of the ecological and water-quality status of aquatic environments. However, only by thoroughly understanding how microorganisms function in healthy aquatic ecosystems can we hope to recognize or accurately predict their responses to water-quality changes. INTRODUCTION Much attention in the field of water quality is focused on microorganisms as indicators of pollution (for example, fecal coliform and fecal streptococci bacteria), threats to public health (for example, pathogenic bacteria and viruses), or symptoms of water-quality deterioration (for example, nuisance algal blooms). Because characteristics common to water quality problems are readily noticeable, the public often receives the mistaken impression that the presence of microorganisms signals the demise of a body of water. As an example, the term "algae" may connote surface scums and foul odors to the layman, while "bacteria" implies disease-causing contamination. In fact, such extreme conditions are rare, and usually occur only in systems which have been altered significantly by excessive loading of nutrients, organic matter, and/or toxic contaminants. Under typical circumstances, microorganisms such as algae and bacteria form vital links in the structure of aquatic ecosystems, and indeed are the operative factors in organic matter production, decomposition, and nutrient regeneration. As professionals in the field of water quality and communicators of water-quality information to other agencies and the general public, it is important to maintain a perspective in regard to the ecological significance of aquatic microorganisms. The purpose of this discussion, therefore, is to review the ecological roles of aquatic microorganisms in lakes and reservoirs. 1/ Biological Station and Department of Zoology, University of Oklahoma, Norman, Oklahoma 73019. AN OVERVIEW OF ECOSYSTEM STRUCTURE Before specifically addressing aquatic microorganisms and their ecological roles, let us briefly consider the basic structure of lentic (that is, lake-like or standing-water) ecosystems. Photosynthetic production usually forms the organic matter base of aquatic foodwebs. Organic matter formed photosynthetically by primary producers (for example, algae) is consumed by herbivores (for example, zooplankton), which are fed upon by higher consumers (carnivores; for example, fish). Predatory transfers, the ingestion and assimilation of living primary producers by herbivores and herbivores by carnivores, collectively are referred to as the "grazer pathway". All of these 'food web levels produce excreted or defecated material and dead organisms which are utilized by "decomposers" (for example, bacteria and fungi). Decomposers promote the breakdown of organic materials to inorganic compounds, and therefore, generally are assigned the role of nutrient regeneration. Non-predatory transfers, which involve the use of non-living organic matter by decomposers, collectively are termed the "detritus pathway" (Fig. 1). Although the flow of energy and materials through both grazer and detritus pathways is recognized, the relative importance of the two pathways in various types of ecosystems appears not to be. It is often generalized that the grazer pathway dominates ecosystem energy flow in grasslands and pelagic (open-water) systems, while the detritus pathway is more important in forests, marshes, and streams. However, this generalization should not be accepted unquestioningly. Although the magnitude of detritus accumulation is obvious in some terrestrial and semi-terrestrial systems in which litter (for example, fallen leaves and dead marsh grass) is readily visible, it is much less apparent in the open waters of lakes and reservoirs where the "litter" (for example, dead algal cells and zooplankton fecal pellets), as well as many of the producers and consumers, is of microscopic size. This discussion considers primarily those aquatic microorganisms which fall into the "Producer" and "Decomposer" categories described above; however, as will be seen, some of these microorganisms also perform roles assignable to "Herbivores" and "Consumers . Our discussion will focus on two fundamental aspects of the ecological roles of microorganisms in lakes and reservoirs: l) Algae as primary producers, and bacteria as decomposers and nutrient regenerators; and 2) Bacteria and fungi as particle producers and potential food sources for higher consumers. ORGANIC MATTER PRODUCTION AND DECOMPOSITION Algae and certain bacteria produce organic matter by the process of photosynthesis, which is the formation of organic compounds from carbon dioxide (C02) and other inorganic nutrients by way of light energy and the chlorophyll pigment in plants. Some bacteria produce organic compounds by chemosynthesis, in which energy- yielding chemical reactions, rather than sunlight, provide the energy necessary for C02 fixation. Both photosynthesis and chemosynthesis result in the formation of organic material from inorganic components, and therefore are considered to be autotrophic (primary production) processes.2/ Although some bacteria are autotrophic, most are heterotrophic and like other heterotrophs (for example, herbivores and higher consumers) they grow by assimilating organic materials previously synthesized by autotrophs. The metabolic processes of all organisms are energy consumptive, and require adenosine triphosphate (ATP, formed during cellular respiration) as their "energy currency". All living organisms, in order to continue living, must conduct cellular respiration, which is in some ways the reverse of photosynthetic carbon fixation (Fig. 2). Organic matter decomposition, a collective term describing the net conversion of organic material back to inorganic compounds (for example, C02, H20, and nutrients), occurs by virtue of the respiratory activities of those heterotrophic microorganisms using the organic material for growth. Carbon dioxide and oxygen are reactants in the photosynthesis- respiration equilibrium (Fig. 2), and the balance or imbalance of these processes within a water body can have profound chemical and biological consequences for the entire system. The photosynthetic production of oxygen is restricted to the upper, lighted regions of the water column (the euphotic zone). Respiration is not directly light-dependent, but is dependent on temperature. Respiration and organic matter decomposition occur through the water column, and depending on the amount of organic matter present and the extent of wind-mixing, can deplete the dissolved oxygen supply in aphotic (unlighted) layers. The chemical and biological conditions associated with such oxygen depletion (for example, increased nutrient release from sediments, exclusion of oxygen-dependent fauna, and less complete decomposition of sedimented organic matter) are marked, and often characteristic of lake trophic status. In oligotrophic (nutrient-poor, unproductive) lakes, insufficient organic matter is produced for decomposition processes to affect available oxygen levels to any significant extent. In contrast, organic matter decomposition in eutrophic (nutrient-rich, productive) lakes can rapidly deplete dissolved oxygen in aphotic parts of the water column. MICROBIAL NUTRIENT TRANSFORMATIONS AND REGENERATION Thus far, organic matter production and decomposition have been discussed primarily in terms of carbon dioxide, water, and oxygen exchanges. However, living-organisms are not composed entirely of C, H, and 0, but also contain small amounts of many other elements. Table 1 compares the elemental composition of living freshwater plants to the environmental availability of elements for plant 2/ However, most chemosynthesis results from energy released in the oxidation of reduced compounds (S-2, NH4+, CH4) derived from the decomposition of previously formed organic matter, and thus is actually a special type of secondary production. A notable exception, where chemosynthesis appears to be a true autotrophic process, is represented by the recently discovered Galapagos Rift hydrothermal vent ecosystems. Here, chemosynthetic bacteria fix C02 with energy derived from the oxidation of geothermically- reduced sulfur compounds emitted from the ocean floor vents (see Karl and others, 1980). Table l.--Concentrations of essential elements for plant growth in the living tissues of freshwater plants (demand), in mean world river water (supply), and the approximate ratio of elemental concentrations required to those available (that is, demand:supply ratio)(after Vallentyne, 1974). DEMAND BY SUPPLY IN DEMAND:SUPPLY ELEMENT SYMBOL PLANTS (%) WATER (%) RATIO Oxygen 0 80.5 89 1 Hydrogen H 9.7 11 1 Carbon C 6.5 0.0012 5,000 Silicon Si 1.3 0.00065 2,000 Nitrogen N 0.7 0.000023 30,000 Calcium Ca 0.4 0.0015 < 1,000 Potassium R 0.3 0.00023 1,300 Phosphorus P 0.08 0.000001 80,000 Magnesium Mg 0.07 0.0004 < 1,000 Sulfur S 0.06 0.0004 < 1,000 Chlorine Cl 0.06 0.0008 < 1,000 Sodium Na 0.04 0.0006 < 1,000 Iron Fe 0.02 0.00007 < 1,000 Boron B 0.001 0.0000l < 1,000 Manganese Mn 0.0007 0.0000015 < 1,000 Zinc Zn 0.0003 0.000001 < 1,000 Copper Cu 0.0001 0.000001 < 1,000 Molybdenum Mo 0.00005 0.0000003 < 1,000 Cobalt Co 0.000002 0.000000005 < 1,000 ~ growth (that is, demand-vs-supply). Phosphorus, nitrogen, and carbon are the least available elements relative to plant growth requirements, and thus are most likely to limit biological productivity in aquatic systems. Although essential nutrients are incorporated into organic compounds during organic matter synthesis, they are regenerated as a result of excretion processes and organic matter decomposition. Organic matter decomposition (Fig. 3) occurs by (1) hydrolysis of large (high molecular weight) organic polymers into smaller (low molecular weight) compounds, and (2) mineralization of these smaller organic molecules to inorganic compounds (for example, H2S, NH4+, and P04 ). Bacterial decomposition of organic materials accounts for a large fraction of the total nutrient regeneration which occurs; however, organisms such as phytoplankton, zooplankton, and fish excrete NH4+, P04 , and low molecular weight organic compounds, and therefore are also important nutrient regenerators. In an oxygenated environment, organic matter exists in a chemically-reduced state (low Eh, high potential energy) relative to most of its inorganic components (Fig. 2). The oxidation of certain mineralization products (for example, S-2 S!Q>S04 -2, NH4+ Q>NO2Q ->N03, and CH4Q>C02) provides the energy for bacterial chemosyntheses. The basic types of microbially-mediated transformations important in carbon, nitrogen, and sulfur cycling are summarized in Tables 2, 3, and 4; and integrated into the overall nutrient cycling patterns for these elements in lake systems in Figures 4, 5, and 6. Phosphorus does not undergo the oxidation-reduction transformations characteristic of C, N, and S cycles (Fig. 7). Inorganic phosphorus occurs in aquatic environments primarily as orthophosphate (P04 -3), and is incorporated directly by algae and bacteria into phospholipids, nucleic acids, and ATP. Although phosphorus turnover time (the time required for phosphorus assimilation and regeneration) is often only a matter of minutes in surface waters during the summer (Lean, 1973), sedimentation of organic particles and precipitation of inorganic phosphorus with iron and manganese complexes can cause phosphorus depletion in the mixed layers of lakes and reservoirs. Naturally low levels of available phosphorus in aquatic environments, the essentiality of phosphorus for plant growth, and the high phosphorus concentration in certain by-products of our modern society (for example, fertilizers, detergents, and municipal sewage) make phosphorus an especially important element in regard to water quality. In short supply, phosphorus availability can severely limit biological productivity, while an overabundance of phosphorus can result in nuisance conditions concomitant with accelerated eutrophication.3/ Since phosphorus is often the least available inorganic nutrient in aquatic environments (that is, relative to demand, see Table 1), extensive efforts have been undertaken in the past decade to minimize phosphorus loading of natural waters. 3/ Eutrophication is a natural process involving the slow accumulation of nutrients and organic matter, and gradually increased productivity in an aquatic system. Accelerated euthrophication results from excessive nutrient loading from the inflow of municipal wastes and/or drainage from fertilized agricultural land, and often is associated with nuisance algal blooms, taste and odor problems, and severe oxygen depletion accompanied by fish kills. Although biogeochemical cycles often are discussed individually by element for the sake of simplicity. it should be realized that in nature they are inseparable. Carbon, nitrogen, sulfur, phosphorus, and other essential elements are assimilated simultaneously during organic matter synthesis, and similarly, are released simultaneously during organic matter decomposition. Because the availability of certain elements (for example, P, Fe, and Mo) influences the uptake or transformations of others (C, N), the elemental cycles are highly interdependent. BACTERIA AS PARTICLE PRODUCERS AND POTENTIAL FOOD SOURCES FOR HIGHER TROPHIC LEVELS The photosynthetic conversion of inorganic compounds to organic matter is only the initial process in a sequence of trophic interactions collectively referred to as "the foodweb". The most familiar foodweb sequence (primary producer > grazer > higher consumer; the grazer pathway) may present an oversimplified view of trophic interactions in lakes and reservoirs by ignoring non- predatory transfers (primary producer > detritus > bacteria > grazer > higher consumer; the detritus pathway). More specifically, the conversion of dissolved organic compounds (derived from algal extracellular excretion or cell lysis, zooplankton excretion, and/or allochthonous sources 4/) to organic particles by way of bacterial uptake and growth represents a potentially important mechanism for reintroducing otherwise unavailable (that is, unharvestable) dissolved organic matter to the foodweb (Fig. 8). For pelagic marine systems, Pomeroy (1974) indicated that the producer-detritus-bacteria-grazer sequence could provide at least 30 percent more energy to higher trophic levels than estimated from consideration of only a producer-grazer pathway. However, whether bacterial secondary production provides a significant source of particulate organic matter for planktonic grazers is a controversial question at present. Free-living (unattached) bacteria are probably too small (