Bopaiah A. Biddanda

Small Players, Large Role: Microbial Influence on Biogeochemical Processes in Pelagic Aquatic Ecosystems

Although prokaryotes are small in size, they are a significant biomass component in aquatic planktonic ecosystems and play a major role in biogeochemical processes. A review of the recent literature shows that the relative importance of prokaryotes to material and energy fluxes is maximized in low-productivity (oligotrophic) ecosystems and decreases in high-productivity (eutrophic) ecosystems. We conclude that competition with eukaryotic autotrophs for dissolved nutrients and competition with phagotrophic heterotrophs and physical processes (sinking, photooxidation) for organic carbon (C) play important roles in determining the relative abundance and impact of prokaryotes in aquatic systems. Oligotrophic systems have low nutrient concentrations, with high proportions of dissolved nutrients in organic form, which favors prokaryotic heterotrophs over phytoplankton. Furthermore, a high proportion of the available organic C is dissolved rather than particulate, which favors prokaryotic heterotrophs over phagotrophic heterotrophs. In eutrophic systems, increased relative concentrations and loading of inorganic nutrients and increased relative concentrations of particulate organic C select for phytoplankton and phagotrophic heterotrophs over prokaryotic heterotrophs. Increased particle sinking fluxes and/or decreased excretion of organic carbon (EOC) may also decrease the relative importance of prokaryotic heterotrophs in eutrophic systems. In oligotrophic systems, interactions between autotrophs and heterotrophs are tightly coupled because the dominant heterotrophs are similar in size and growth rates, as well as having similar nutrient composition to the dominant autotrophs, small phytoplankton. In eutrophic systems, increased productivity passes through zooplankton that are larger and have slower growth rates than the autotrophs, leading to a greater potential for decoupled auto- and heterotrophic production and increased export production.

Abundance, size distribution, and stable carbon and nitrogen isotopic compositions of marine organic matter isolated by tangential-flow ultrafiltration

Tangential-flow ultrafiltration was used to isolate particulate and high-molecular-weight dissolved material from seawater collected at various depths and geographic regions of the Pacific and Atlantic Oceans. Ultrafiltration proved to be a relatively fast and efficient method for the isolation of hundreds of milligrams of material. Optical and electron microscopy of the isolated materials revealed that relatively fragile materials were recovered intact. Depth-weighted results of the size distribution of organic matter in seawater indicated that ~ 75% of marine organic carbon was low-molecular-weight (LMW) dissolved organic carbon ( 100 nm). The distribution of carbon in surface water was shifted to greater relative abundances of larger size fractions, suggesting a diagenetic sequence from macromolecular material to small refractory molecules. The average C:N ratios of particulate organic matter (POM) and HMW dissolved organic matter (DOM) were 7.7 and 16.7, respectively. Differences in C:N ratios between POM and HMW DOM were large and invariant with depth and geographic region, indicating that the aggregation of HMW DOM to form POM must be of minor significance to overall carbon dynamics. The stable carbon isotope composition (δ13C) of POM averaged −22.7%. in surface water and −25.2%. in subsurface water. Several possible explanations for the observed isotopic shift with depth were explored, but we were unable to discern the cause. The δ13C of HMW DOM samples was relatively constant and averaged −21.7%., indicating a predominantly marine origin for this material. The δ15N values of POM were highly variable (5.8–15.4%.), and the availability of nitrate in surface waters appeared to be the major factor influencing δ15N values in the equatorial Pacific. In the upwelling region nitrate concentrations were relatively high and δ15N values of POM were low, whereas to the north and south of the upwelling nitrate concentrations were low and δ15N values were high. The δ15N values of HMW DOM reflected the same trends observed in the POM fraction and provided the first such evidence for biological cycling of dissolved organic nitrogen (DON). Using the observed δ15N values and an estimate of meridional advection velocity, we estimated a turnover time of 0.3 to 0.5% day−1 for HMW DON. These results suggest a major role for DON in the upper ocean nitrogen cycle.

Love Handles in Aquatic Ecosystems: The Role of Dissolved Organic Carbon Drawdown, Resuspended Sediments, and Terrigenous Inputs in the Carbon Balance of Lake Michigan

During the unstratified (winter) and stratified (summer) periods of 1999 and 2000, we examined carbon (C) dynamics in the upper water column of southern Lake Michigan. We found that (a) bacterial respiration (BR) and planktonic respiration (PR) were major sinks for C, (b) C flux through bacteria (CFTB) was diminished in winter because of reduced bacterial production (BP) and increased bacterial growth efficiency (BGE) at colder temperatures, and (c) PR exceeded primary production (PP) during the spring–summer transition. Drawdown of dissolved organic C (DOC), resuspended organic matter from the lake floor, and riverine organic matter likely provided organic C to compensate for this temporal deficit. DOC in the water column decreased between winter and summer (29–91 mg C m2 d−1) and accounted for 20%–53% of CFTB and 11%–33% of PR. Sediment resuspension events supported elevated winter heterotrophy in the years that they occurred with greatest intensities (1998 and 2000) and may be important to interannual variability in C dynamics. Further, riverine discharge, containing elevated DOC (5×) and dissolved P (10×) relative to lake water, peaked in the winter–spring season in southern Lake Michigan. Collectively, terrigenous inputs (river, stream, and groundwater discharges; storm water runoff; and atmospheric precipitation) may support approximately 10%–20% of annual in-lake heterotrophy as well as autotrophy. Terrestrial subsidies likely play a key role in the C balance of even very large lakes, representing a critical linkage between terrestrial and aquatic ecosystems.

Organic carbon biogeochemistry of Lake Superior

We examined the organic carbon budget for the Earths largest lake, Lake Superior, in the Laurentian Great Lakes. This is a unique, ultra-oligotrophic system with many features similar to the oligotrophic oceanic gyres, such as dominance of microbial biomass and dissolved organic carbon in biogeochemical processes. Photo-autotrophy is the dominant source of reduced organic matter in the lake. Areal rates of primary production are among the lowest measured in any aquatic system, and are likely a result of cold water temperatures and low nutrient concentrations in the lake. Allochthonous riverine organic carbon inputs were estimated at about 10 percent of photo-autotrophic production. Atmospheric carbon deposition has not been measured to any significant extent but we estimate it at 0.16 to 0.41 Tg yr−1 . All together, allochthonous carbon sources provide 13 to 19 percent of photo-autotrophic production. The main loss of organic matter in the lake is through respiration in the water column. Respiration is double all estimated organic carbon sources combined and therefore sources are likely underestimated. Few measurements of photo-autotrophic carbon production have been made and none recently. Nonetheless, most of the production and fluxes in this system pass through the large dissolved organic carbon pool (more than 10 times as large as the particulate organic carbon pool), which is mediated by heterotrophic and autotrophic picoplanktonic microbial flora. Improved understanding of dissolved organic carbon pools and dynamics is critical for constraining carbon flux in ultra-oligotrophic Lake Superior.

Temperature affects stoichiometry and biochemical composition of Escherichia coli

Temperature is a master variable controlling biochemical processes in organisms, and its effects are manifested on many organizational levels in organisms and ecosystems. We examined the effects of temperature on the biochemical composition and stoichiometry of a model heterotrophic bacterium, Escherichia coli K-12, held at constant growth rate in chemostats. Increasing temperature led to increased cellular organic carbon (C) and organic nitrogen (N) with decreased phosphorus (P) content, leading to increased C/P and N/P biomass ratios. P content was related to cellular RNA, which is P-rich (9–10% by weight) and nonnucleic acid P (presumably composed of mostly phospholipids, intracellular phosphate, and polyphosphate). These results indicate that E. coli allocates an increased proportion of its P cell quota toward assembly (ribosomes) at low temperatures and an increasing proportion toward resource acquisition machinery (membranes) at higher temperatures. If these results are relevant to the behavior of prokaryotic heterotrophs in natural settings (the gut, soils, lakes, oceans, etc.), it suggests greater nutrient regeneration and less microbial nutrient retention as temperatures increase.

Enhancement of Dissolved Organic Matter Bioavailability by Sunlight and Its Role in the Carbon Cycle of Lakes Superior and Michigan

The degree to which sunlight and microbes interact in the cycling of dissolved organic matter (DOM) of natural waters is unclear. During 1999 and 2000, the effects of sunlight on the lability of DOM in two of the Laurentian Great Lakes were examined. Bacteria-free (< 0.2 μm) water samples collected in Lake Superior and Lake Michigan were exposed to ambient sunlight for several days and subsequently inoculated (1:10) with < 1.0 μm lake water containing natural bacteria and assayed for bacterial growth rates (3H-leucine incorporation into protein) in the dark. Exposure of water collected from offshore surface layers to sunlight caused a net reduction of DOM bioavailability (bacterial growth ∼20 to 30% of dark control), whereas both exposure of deep water and river water to sunlight resulted in a net enhancement of DOM bioavailability (bacterial growth ∼150 to 260% of dark control). Irradiated water from nearshore exhibited an intermediate response in terms of changes in DOM bioavailability (bacterial growth ∼75 to 115% of dark control). Despite the reduction of DOM bioavailability in surface waters by sunlight exposure in the short-term (relative to dark control), subsequent incubation of these waters in the dark increased bacterial production rates relative to in situ rates, suggesting that the net effect of exposure to sunlight, even in surface waters, was to increase DOM bioavailability. Rapid and sustained photochemical alterations of DOM bioavailability occurring in the euphotic zone of natural waters should accelerate the turnover of surface water, older deep water, and refractory terrigenous carbon.

Current Status and Trends in Muskegon Lake, Michigan

ABSTRACT A long-term monitoring program was initiated in 2003 to determine the ecological status of Muskegon Lake, a Great Lakes Area of Concern. This paper presents data generated from the first 3 years of the monitoring program, discusses how the data are being used to establish and justify lake restoration targets, and assesses how water quality conditions have changed over time. Between 1972 and 2005, lake-wide averages of total phosphorus and soluble reactive phosphorus from the water surface have declined from 68 to 27 μg/L and from 20 to 5 μg/L, respectively. In addition, average chlorophyll α concentrations have declined from 25 to 6 μg/L over this period, while Secchi disk depths have increased from 1.5 to 2.2 m. Wastewater diversion, and perhaps dreissenid filtering activity, is most likely responsible for these changes. However, nitrate concentrations have increased from 70 to 270 μg/L over the same time period. During 2003–2005, phytoplankton abundance and fish catch were lower in the spring compared to the summer and fall. Microcystis was the most abundant phytoplankton genus; the fish community generally was dominated by round goby (Neogobius melanostomus) in spring and summer, and sunfishes (Centrarchidae) in the fall. Dreissenid abundance was highly variable over time, but densities were low relative to Saginaw Bay. Approximately 65% of the Muskegon Lake shoreline has been hardened (i.e., physically altered). Overall, the water quality of Muskegon Lake has improved over the past 30 years, but environmental challenges still exist, including contaminated sediments, loss of natural habitat, and invasive species.

Occurrence of the Toxin-producing Cyanobacterium Cylindrospermopsis raciborskii in Mona and Muskegon Lakes, Michigan

ABSTRACT The bloom-forming and toxin-producing cyanobacterium Cylindrospermopsis raciborskii was observed in Muskegon and Mona lakes, drowned river-mouth tributaries of Lake Michigan. Morphological features of the taxon were similar to those described elsewhere. The species was observed only in late summer; elevated bottom water temperature, and perhaps phosphorus concentration, appears to be implicated in its appearance. Maximum abundances at any given site reached 393 and 0.9 trichomes/mL in Mona Lake and Muskegon Lake, respectively. Although these concentrations are low relative to other reports, the presence of this species in these two lakes from adjacent watersheds adds to a growing body of literature that suggests the distribution of C. raciborskii is on the increase in northern latitudes.

The role of free and attached microorganisms in the decomposition of estuarine macrophyte detritus

Abundance and respiration of free and attached microorganisms were monitored during the decomposition of the seagrass Scirpus maritimus leaves in laboratory microcosms for 30 days. There was a clear succession between bacteria and heterotrophic flagellates during the course of the study. The beginning of the study (1-4 days) was characterized by higher rates of bacterial respiration, compared to the later periods. Free microorganisms were responsible for more than half of the respiration (65%) within the microcosms, suggesting that they were responsible for the mineralization of the bulk of the macrophyte detritus following its dissolution. On the other hand, estimates of activity on a per cell basis revealed that individual attached bacteria had much higher (3- to 4-fold) respiration rates than free bacteria, suggesting attached bacterial activity may play a key role in the breakdown and dissolution of particulate detritus in estuarine waters. The findings suggest different but coupled roles for attached and free bacteria in nature.

Major contribution from mesopelagic plankton to heterotrophic metabolism in the upper ocean

Abstract Measurements of plankton respiration and heterotrophic bacterial abundance and production were made at seven deep water stations within the upper 500 m of the Gulf of Mexico during the summer of 1995. Bacterial abundance [(1.1–4.6)×108 1−1] and rates of bacterial production (2–19 nM C h−1) and plankton respiration (50–245 nM O2 h−1) decreased with depth by four- to nine-fold, and were similar to those reported for oligotrophic waters. Bacterial turnover times increased with depth from approximately 1 to 5 days. Bacterial growth efficiencies decreased from 15% at the surface to 8% at 500 m. Depth-integrated plankton respiration exceeded known estimates of primary production for the region, suggesting that heterotrophic utilization of previously and concurrently produced organic matter (e.g. spring phytoplankton growth, and summer blooms of Trichodesmium sp.) was occurring during the summer. Estimates for the upper 500 m showed that roughly half of the bacterial biomass (56%), bacterial production (49%), and plankton respiration (60%) occurred below the euphotic zone. Routine oceanographic studies have focused exclusively on the metabolic activity occurring within the euphotic zone. Our measurements, however, indicate that mesopelagic plankton also contribute substantially to heterotrophic metabolism and nutrient cycling in the ocean.