Jorgensen, B. 1978. A comparison of methods for the quantificationof bacterial sulfate reduction in coastal marine sediments. 1. Mea-surement with radiotracer techniques. Geonicrohiology Journal, 1, 11-27.

Lawrence, M.J.F., and C. H. Hendy. 1985. Water column and sedimentcharacteristics of Lake Fryxell, Taylor Valley, Antarctica. New ZealandJournal of Geology and Geophysics, 28, 543-552.

Lawrence, M.J.F., and C.H. Hendy. 1989. Carbonate deposition andRoss Sea ice advance, Fryxell basin, Taylor Valley, Antarctica. NewZealand Journal of Geology and Geophysics, 32, 267-277.

Li, Y.-H., and S. Gregory. 1974. Diffusion of ions in seawater and indeep-sea sediments. Geochi,nica et Cosinochimica Acta, 38, 703-714.

Toni, T., N. Yamagata, S. Nakaya, S. Murata, T. Hashimoto, 0. Mat-subaya, and H. Sakai. 1975. Geochemical aspects of the McMurdosaline lakes with special emphasis on the distribution of nutrientmatters. In T. Toni (Ed.), Memoirs of National Institute of Polar Research:Geochemical and Geophysical Studies of Dry Valleys, Victoria Land inAntarctica. (Special Issue No. 4.)

Vincent, W.F. 1981. Production strategies in Antarctic inland waters:Phytoplankton eco-physiology in a permanently ice-covered lake.Ecology, 62, 1,215-1,224.

Wharton, R.A., C.P. McKay, G.M. Simmons, and B.C. Parker. 1986.Oxygen budget of a perennially ice-covered Antarctic lake. Limnologyand Oceanography, 31, 437-443.

Bacterial biomassand heterotrophic activity

in the water columnof an amictic antarctic lake

RICHARD L. SMITH

Water Resources DivisionU.S. Geological SurveyDenver, Colorado 80225

BRIAN L. HOWES

Biology DepartmentWoods Hole Oceanographic InstituteWoods Hole, Massachusetts 02543

The lakes in the McMurdo Dry Valleys have several uniquephysical characteristics that make them unusual environmentsfor aquatic microorganisms. The thick, permanent ice cover onthese lakes maintains a constant temperature within each lakeby insulating the water column. The ice also markedly reduceslight penetration and prevents exchange of gases and nutrientsbetween the water column and the atmosphere (Vincent 1981;Wharton et al. 1986). Many of the dry valley lakes contain largesalinity gradients that extend vertically throughout the entirewater column, and these gradients effectively prevent mixingfrom occurring (Toni et al. 1975). Lakes of this type are rareexamples of true amixis and, as such, are systems in whichsolute movement is predominantly a diffusion-controlled pro-cess. The lakes are situated in closed-basin drainages notedfor their barren moonscape appearance and the nearly com-plete absence of any plants and animals. Hydrologic rechargeto the lakes occurs only during a 6-8-week period from glacialmeltwater and does not contain significant concentrations ofdissolved organic matter or nutrients (Howard-Williams, Priscu,and Vincent 1989; Green, Angle, and Chave 1988). In essence,these lakes may represent the natural environment that mostclosely approximates a closed aquatic ecosystem; systems thatare controlled entirely by internal processes.

We are studying the biogeochemical processes affecting thecarbon, nitrogen, and sulfur cycles within one of these dryvalley lakes, Lake Fryxell (77°37'S 163°8'E). A part of the study

involves enumerating and characterizing the total microbialpopulations within the lake. Little is known about microor-ganisms in such systems, especially the planktonic bacteria,even though it appears that much of the carbon, nitrogen, andsulfur cycling may occur in the water column (Canfield andGreen 1985; Vincent, Downs, and Vincent 1981).

Lake Fryxell is one of the most productive lakes in theMcMurdo Dry Valleys (Vincent 1981). It contains a relativelyuniform salinity gradient and a corresponding increase in dis-solved organic matter with depth. The dissolved organic mat-ter reaches a maximum concentration of 25 milligrams of carbonper liter at 18 meters (maximum depth, 18.5 meters) (McKnightet al. 1988). The water column is composed of an upper aerobiczone that contains oxygen concentrations well in excess ofatmospheric equilibrium and an anoxic zone that contains re-duced compounds such as ammonium (figure 1), hydrogensulfide, and methane (data not shown). The oxycline, the re-gion of transition between these two zones, has a very steepoxygen gradient; dissolved oxygen values decrease from 0.9to 0 millimoles per liter in only 1.5 meters (from 8.0 to 9.5meters). Very high oxygen concentrations within the zone oflight penetration have been found in other antarctic lakes andresult because the ice cover restricts exchange of gases withthe atmosphere (Wharton et al. 1986). Immediately beneaththe oxic-anoxic interface in Lake Fryxell there is a turbiditymaximum (9.5 meters, figure 1). At least part of this highturbidity was due to populations of bacteria. Bacterial abun-dance increased dramatically from 9.0 to 10.5 meters, with apeak value at 10.5 meters that was nearly eightfold greaterthan that in the aerobic portions of the water column (figure2). Morphologically, the bacteria were much larger within thisdepth interval than elsewhere in the depth profile, which wouldalso help account for the turbidity maximum. Interestingly,bacterial abundance was 2-3 times higher in the deeper, anoxiczones (12-18 meters) than in the aerobic zone, a phenomenonthat has also been reported for a saline, meromictic, temperatelake (Zehr et al. 1987) and may be the result of grazing byprotozoan populations in the aerobic zone.

In general, the microbial populations within Lake Fryxellwere physiologically stressed. The adenylate energy chargevalues for planktonic microorganisms throughout most of thedepth profile were 0.5-0.6 (figure 2), indicative of a starvingor extremely stressed metabolism. The energy charge of a cellestimates the energy potential of the cell in a manner analogousto a battery potential; the theoretical range is 0-1, but the actuallimits for pure cultures are 0.4-0.5 for dying or senescing cellsand 0.75-0.8 for exponential growth (Atlas and Bartha 1981).

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II-.a-

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46810TURBIDITY (NTu)

Figure 1. Depth profiles in December 1987 in Lake Fryxell of dis-solved oxygen, ammonium, and turbidity. Turbidity was measuredwith a nephelometer. (NTU denotes national turbidimetric units. mdenotes meter. mM denotes millimole per liter.)

Figure 2. Depth profiles in December 1987 in Lake Fryxell of bac-terial abundance and adenylate energy charge of the total microbialpopulation. Bacterial abundance was determined by epifluoresc-ence microscopy (Harvey 1987). Adenylate energy charge (EC) wascalculated from: EC =(ATP + 1/2ADP)/(ATP + ADP + AMP). The ATP,ADP, and AMP content in the bacterial biomass was determinedaccording to the method of Walker et al. (1986). (m denotes meter.ml denotes milliliter.)

There were two depths in Lake Fryxell in early December 1987that exhibited energy charge values characteristic of activelygrowing populations of microorganisms (figure 2). A 7-meterpeak in energy charge correlated with the lowest bacterialabundance in the entire water column. There was, however,a peak in chlorophyll concentrations at this depth and a cor-responding peak of phytoplankton, which was primarily com-posed of Oscillatoria sp. (McKnight et al. 1988). The Oscillatoriabiomass would significantly "swamp out" the bacterial bio-mass in the energy charge calculation at the 7-meter depthbecause of the greater amount of total adenylates per cell forphytoplankton versus bacteria. The Oscillatoria in Lake Fryxellwas probably in the midst of a bloom, and hence the higherenergy charge, which might be expected given the rapid in-crease in photosynthetically active radiation in the Dry Valleysduring the month of November (Simmons, McKay, and Whar-ton 1987).

The deeper of the two energy-charge peaks (9.5-10.0 meters)suggests that the bacteria in the turbidity maximum were alsoactively growing, which would account for their larger cell size.In addition, these organisms demonstrated the greatest het-erotrophic activity within the water column (figure 3). Ratesof 3H-glucose uptake (at 1 micromole per liter glucose) wereover 10 times greater within the 9.5-10.0-meter interval thanfor samples collected from any other depth interval. As noted,these organisms are situated at the oxic-anoxic interface and,therefore, benefit from the flux of reduced constituents, such

as ammonium, from below, and degradable organic matterfrom oxygenic photosynthesis occurring above, as well as che-mosynthesis and anoxic photosynthesis within the intervalitself. Other heterotrophic activity measurements with 3H-ac-etate (data not shown) resulted in a depth profile very similarto that of the 3H-glucose uptake. In general, heterotrophicactivity was very low below 12 meters and above 8 meters,which together constitute 75 percent of the water column,while 75.3 percent of the integrated heterotrophy was foundin the 8.5-12.0-meter interval. Interestingly, there were nosignificant increases in heterotrophy in the depth intervals inwhich photosynthesis was actively occurring (figure 3).

On an areal basis, the total carbon turnover, due to microbialmetabolism as measured by 3H-glucose uptake, was 1.97 mil-limoles of carbon per square meter per day. This compareswith a total amount of dissolved organic matter within thewater column of 14.9 moles of carbon per square meter. 3H-glucose uptake does not reflect the turnover of the total dis-solved organic matter pool, and the lability of the various com-ponents of dissolved organic matter is undoubtedly substantiallydifferent because glucose is only a very small component ofthat pool. However, glucose does not represent that fractionof the dissolved organic matter pool that is readily utilized bymicroorganisms, and in that regard, glucose update can beuseful as a first approximation for estimating the flux or re-moval rate of dissolved organic carbon by microorganisms whenconstructing a carbon budget. The rate of this flux component

234 ANTARCTIC JOURNAL

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Figure 3. Depth profile in December 1987 in Lake Fryxell of the rateof 3H-glucose uptake for water samples amended with 1 micromoleper liter glucose and incubated for 20 hours in the dark as describedby Smith, Harvey, and LeBlanc (in press). (m denotes meter. nmolL 1 hr' denotes nanomoles per liter per hour.)

in Lake Fryxell is such that it would take more than 20 yearsto remove an amount of carbon equivalent to the current stand-ing stock of dissolved organic matter from the water columnof the lake. It is important to keep in mind that dissolvedorganic matter, however, is also being continually added tothe water column by primary and secondary productivity, bydiffusion from the sediments, and by degradation of particu-late organic matter within the water column. These differentsources of dissolved organic matter will undoubtedly havedifferent residence times in the lake and different removal ratesby microoganisms. Because of the unique light-dark cycle inantarctic lakes, the effect of some of these differences uponheterotrophic activity should be most evident during the dark-ness of the austral winter after primary productivity has stopped.Thus, measurements of dissolved organic matter and hetero-trophic activity during this period could add valuable insightinto carbon cycling within antarctic lakes.

We thank J . Duff and L. Miller for assistance in the field andR. Harvey for bacterial enumeration and M. Brooks for ade-nylate analysis. This research was supported by the U.S. Geo-logical Survey and by National Science Foundation grant DPP86-13607.

Woods Hole Oceanographic Institution contribution number7441.

References

Atlas, R.M., and R. Bartha. 1981. Microbial ecology. Reading, Massa-chusetts: Addison-Wesley.

Canfield, D.E., and W.J. Green. 1985. The cycling of nutrients in aclosed-basin Antarctic lake: Lake Vanda. Biogeochemistry, 1, 233-256.

Harvey, R.W. 1987. A fluorochrome-staining technique for countingbacteria in saline, organically-enriched, alkaline lakes. Limnology andOceanography, 32, 993-995.

Howard-Williams, C., J.C. Priscu, and W.F. Vincent. 1989. Nitrogendynamics in two antarctic streams. Hydrohiologia, 172, 51-61.

Green, W.J., M.P. Angle, and K.E. Chave. 1988. The geochemistry ofAntarctic streams and their role in the evolution of four lakes of theMcMurdo Dry Valleys. Geochi?nica et Cosmochimica Acta, 52, 1,265-.1,274.

McKnight, D.M., G.R. Aiken, E.D. Andrews, E.C. Bowles, R.L. Smith,J. H. Duff, and L. G. Miller. 1988. Dissolved organic material in desertlakes in the McMurdo Dry Valleys. Antarctic Journal of the U.S., 23(5),152-153.

Simmons, G.M., Jr., C.P. McKay, and R.A. Wharton, Jr. 1987. Icethickness changes on Lake Hoare, southern Victoria Land, Antarc-tica. Antarctic Journal of the U.S., 22(5), 235-236.

Smith, R.L., R.W. Harvey, and D.L. LeBlanc. In press. Use of close-interval sampling in delineating chemical and microbiological gra-dients in contaminated aquifers. Journal of Contaminant Hydrology.

Toni, T., N. Yamagata, S. Nakaya, S. Murata, T. Hashimoto, 0. Mat-subaya, and H. Sakai. 1975. Geochemical aspects of the McMurdosaline lakes with special emphasis on the distribution of nutrientmatters. In T. Toni (Ed.), Geochemical and geophysical studies of DryValleys, Victoria Land in Antarctica. Tokyo, Japan: National Instituteof Polar Research.

Vincent, W.F. 1981. Production strategies in antarctic inland waters:Phytoplankton eco-physiology in a permanently ice-covered lake.Ecology, 62, 1,215-1,224.

Vincent, WE., M.T. Downes, and C.L. Vincent. 1981. Nitrous oxidein Lake Vanda, Antarctica. Nature, 292, 618-620.

Walker, G.S., M.F. Coveney, M.J. Kiug, and R.G. Wetzel. 1986. Iso-cratic HPLC analysis of adenine nucleotides in environmental sam-ples. Journal of Microbiological Methods, 5, 255-264.

Wharton, R.A., Jr., C.P. McKay, G.M. Simmons, Jr., and B.C. Parker.1986. Oxygen budget of a perennially ice-covered antarctic dry valleylake. Limnology and Oceanography, 31, 437-443.

Zehr, J.P., R.W. Harvey, R.S. Oremland, I.E. Cloern, L.H. George,and J.L. Lane. 1987. Big Soda Lake (Nevada). 1. Pelagic bacterialheterotrophy and biomass. Limnology and Oceanography, 32, 781-793.

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