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~IN SITU NITROGEN(C H )-FIXATION IN LAKES OF 2 2 SOUTHERN VICTORIALAND, ANTARCTICA 1 by F.C. Thomas Allnutt, .._\ )I Thesis submitted to the Graduate Faculty of the Virginia Polytechnic Institute and State University in partial fulfillment of the requirements of the degree of Master of Science of Microbiology APPROVED: B.C. Parker, Chairman R.E. Benoit / J-S. Chen 1 R.A. Paterson ACKNOWLEDGEMENTS My appreciation for a job well done is expressed to the following members of the Antarctic field teams: ' , and The technical and motivational assist- ance of the following persons was considerable: , and The cooperation of in algal identifications and unialgal experi- mentation was profitable and appreciated. The advice and assistance of the following professors aided in the pursuit of this degree: and is especially thanked for the aid and harangue received during this project. Logistical support provided by the National Science Foundation, the U.S. Navy (VXE - 6) and and was necessary for implimentation of this research. Financial support for this research was off NSF grant DPP 76-23996. ii TABLE.OF CONTENTS Page ACKNOWLEDGEMENTS • • • ii LIST OF TABLES • • v LIST OF FIGURES • • • • • • • • • • • • • • • • • • • • • • • • • vi I. INTRODUCTION ••• 1 II. LITERATURE REVIEW 2 Nitrogen Fixation - General • • • • • • • • • • • • • • 2 Antarctic Nitrogen Fixation • • • • • • • • • • • • • • 4 Assay Techniques for Nitrogen Fixation • • • • • • • • • 5 III. MATERIALS AND METHODS ••• 8 Physical Measurements • • • • • • • • • • • • 8 Water Chemical Analyses • • • • • • 8 Field Collections and Culturing • • • • • • • • • • 10 Acetylene Reduction • • • • • • • • • • • • 11 Method I - Serum Bottles • • 11 Method II - SARAN Bag Chambers • 13 Method III - Sediment Coring Apparatus • • • • 14 15N2-Uptake Assay • • • • • • • • • • • • • • • • • • • 14 Statistical Analysis • • • • • • • • • • • • • • • • • • 16 IV. SITE DESCRIPTION - LITERATURE REVIEW • • • • • • • • • • • • 17 V. RESULTS AND DISCUSSION • • • • • • • • • • • • • • • • • • • • 25 C2H2 Reduction Data • • • • • • • • • • • • • • • • • • 26 Soils • • • • • • • • • • • • • • • • • • • • • • • 26 Plankton . 30 Littoral Moat Algal Mats • • • • • • • • • • • • • 30 Peripheral Habitats • • • • • • • • • • • • • • • • 35 Benthic Algal Mats • • • • • • • • • • • • • • • • 35 Habitat Descriptions • • • • • • • • • • • • • • • • • • 36 Littoral Moat Co11D11unities • • • • • • • • • • • • • 36 Co11D11unities of Lake Peripheral Regions • • • • • • 41 Benthic Co11D11Uni ty • • • • • • • • • • • • • • • • • 46 15N Fixation Attempts • • • • • • • • • • • • • • • • • 51 VI. CONCLUSIONS • • • •• 52 VII. LITERATURE CITED • • 54 iii Page VIII. APPENDICES 1. Eukaryotic Algal Species in the Algal Mats of Lake Fryxell, 1978-79 Austral SuID1Der • • • • • • • • • • • • • • • • • • • • • • 60 2. Eukaryotic Algal Species in the Algal Mats of Lake Chad, 1978-79 Austral SuUDner • • • • 62 3. Eukaryotic Algal Species in the Algal Mats of Lake Hoare, 1978-79 Austral Summer • • • • 64 4. Bluegreen Algal (Cyanobacterial) Species as a Percentage of Total Cell Number in the Algal Mats of Lake Fryxell, 1978-79 Austral SUDJm.er . • . • • • . • • . • . 65 5. Bluegreen Algal Species as a Percentage of Total Cell Number in the Algal Mats of Lake Chad, January 26, 1979 ••••••• 67 6. Bluegreen Algal {Cyanobacterial) Species as a Percentage of Total Cell Number in the Algal Mats of Lake Hoare, 1978-79 Austral Sunnner . 69 7. Site Descriptions of the Areas Studied During the 1977-78 and 1978-79 Austral SlDIDDers • • • • • • • • • • • • • • • • 70 8. Method for Qualitative Determination of Oyxgen in Mats • • • • • • • • • • • • • • • • 76 9. Standing Crop of Various Algal Mat COUDnunities of Lakes Chad, Fryxell and Hoare, 1978-79 Austral Summer 78 IX. VITA ••• . 79 ABSTRACT iv LIST OF TABLES Page 1. Summary of physical data for seven Southern Victorialand lakes • • • • • • • • • • • • • • • • • 22 2. Acetylene reduction rates at four temperatures and different incubation times (h) using a unialgal culture of Anabaena aequalis isolated from Lake Miers, Antarctica • • •••••• . 28 3. A qualitative survey of c2H2 reduction in a number of habitats in Southern Victorialand lakes, 1977-78 austral sunnner •••• 29 4. Nitrogen(C2H2)-fixation rates from in situ incubations of bluegreen algal mats of Lakes Chad, Fryxell and Hoare, 1978-79 austral summer ••• 32 5. Light and dark c2H2 reduction in Lake Fryxell's littoral moat algal mat, January 1979 • • • 34 6. Dissolved and total organic carbon, anunonia and nitrates found in the waters of the sites studied during the 1978-79 austral sunnner ••••• 38 7. Dominant bluegreen algal species, acetylene reduction and presence of heterocystous bluegreen algae at sites studied during the 1978-79 austral sUID111er • • • • • • • • • • • • • • 42 8. Physical measurements from the water above benthic mats in Lake Fryxell and Lake Hoare, 1978-79 austral sunnner • • • • • • • • • • • • • • • • • 4 7 v LIST OF FIGURES Page 1. SARAN bag assay chamber for acetylene reduction on soil samples (Burris, 1974) •••••••• 15 2. Southern Victorialand, Antarctica, with inset maps of lakes studied during the 1977-78 and 1978-79 austral sunnners • • • • • • • • • • •• 18 3. Diagram showing the study sites on Lakes Chad, Fryxell and Hoare during the 1978-79 austral summer. This map removed from a United States Geological Survey map • • • • • • • • • • • 23 4. Acetylene reduction versus temperature in a unialgal culture of Anabaena aequalis isolated from Lake Miers, Antarctica • • • • • • •• 27 5. Schematic representation of the littoral moat and benthic regions of Lakes Fryxell and Hoare • • • • • • • • 37 6. Heterocystous bluegreen algae found in algal mats of Lakes Chad, Fryxell and Hoare (right, Anabaena sp., left, Nostoc coDDllune) ••••• 39 7. Bluegreen algal mat cODDllunities from the littoral moat and peripheral regions. From upper right hand corner clockwise: littoral moat mat of Lake Bonney, littoral moat mat from Lake Fryxell, littoral moat mat from Lake Chad, and peripher~l water mat from Lake Fryxell • • • • • • • • 44 8. Benthic or attached algal coDDllunity beneath the permanent ice layer of Lake Hoare • • • • • • • • • • • • • • 48 9. Coring Apparatus for determination of oxygen content within algal mats • • • • • • • • • • 77 vi INTRODUCTION Primary production in antarctic habitats may be limited by nitrogen (Goldman, 1970; Samsel and Parker, 1971, 1972), phosphorus (Hoehn et al., 1977), and for some organisms perhaps silicon (Parker et al., 1972; Seaburg et al., 1979). In addition the biota also may be subjected to low temperature, light and moisture (Parker, 1978). If there is a ni- trogen deficiency in these habitats, it should play an important role in cormnunity development, which may indicate the presence of nitrogen fix- ing organisms. Studies in subantarctic island lakes and terrestrial habitats have shown nitrogen fixation in the algal mat cormnunity (Croome, 1973; Fogg and Stewart, 1968; Horne, 1972), while in situ ni- trogen fixation on the antarctic continent has not been reported pre- viously. The objectives of this study included the determination of the ex- tent of nitrogen fixation in select habitats in Southern Victorialand and the identification of the key organisms involved. The habitats studied were littoral or temporary ice-free moat areas, soils and plank- ton of a number of lakes during the 1977-78 austral summer. Also, the investigation included a more intensive evaluation of lakes Chad, Hoare, and Fryxell during the 1978-79 austral surmner which added the benthic attached algal mat as a study site. Another aim of this study was to identify any spatial patterns of nitrogenase activity within the lakes. 1 LITERATURE REVIEW Nitrogen Fixation - General Biological nitrogen fixation is the reduction of nitrogen gas (N ) 2 to alllllonia (NH ) catalyzed by the nitrogenase enzyme complex. Nitrogen- 3 ase receives electrons from a donor molecule (e.,&.., pyruvate) via a carrier molecule (e._&., ferredoxin) to reduce the triple bonded N by 2 adding six hydrogen atoms (H) to synthesiie annnonia. Energy as 12 to 24 molecules of adenosine triphosphate (ATP) is expended per molecule of N reduced. Recycling of reducing power from H may allow more effi- 2 2 cient utilization of this energy. Numerous authors have reviewed the biochemistry of N2 fixation which will not be further discussed here (Mortenson and Thorneley, 1979; Orme-Johnson and Davis, 1977; Winter and Burris, 1976; Zumft and Mortenson, 1975). Certain bluegreen algae and bacteria fix N2 as free-living organ- isms or in symbiotic associations. Symbioses involving bacteria or bluegreen algae with higher plants and fungi are considered responsible for at least 50% of the total worldwide N2 fixation, as reviewed by Postgate (1972). The correlation of aerobic N2 fixation in bluegreen algae with the presence of heterocysts is well-known (Fogg, 1944, 1949, 1951). In fact, heterocysts probably are the site of N2 fixation in most bluegreen algae (Fay, 1973; Wolk, 1974). Anaerobic or microaerophilic N2 fixation has been observed in non-heterocystous bluegreen algae, as well as, the filaments of heterocystous algae (Fogg, 1974). Oxygen apparently inac- tivates nitrogenase activity, which is countered by the differentiated 2 3 heterocysts. Dark N fixation is common among heterotrophic bacteria, but only 2 recently has evidence been provided for dark N fixation by bluegreen 2 algae (Khoja and Whitton, 1971). Fogg (1974) has reviewed the evidence
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