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The Role of Bacterioplankton in Lake Erie Ecosystem Processes: Phosphorus Dynamics and Bacterial Bioenergetics

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The Role of Bacterioplankton in Lake Erie Ecosystem Processes: Phosphorus Dynamics and Bacterial Bioenergetics THE ROLE OF BACTERIOPLANKTON IN LAKE ERIE ECOSYSTEM PROCESSES: PHOSPHORUS DYNAMICS AND BACTERIAL BIOENERGETICS A dissertation submitted to Kent State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Tracey Trzebuckowski Meilander December 2006 Dissertation written by Tracey Trzebuckowski Meilander B.S., The Ohio State University, 1994 M.Ed., The Ohio State University, 1997 Ph.D., Kent State University, 2006 Approved by __Robert T. Heath___________________, Chair, Doctoral Dissertation Committee __Mark W, Kershner_________________, Members, Doctoral Dissertation Committee __Laura G. Leff_____________________ __Alison J. Smith____________________ __Frederick Walz____________________ Accepted by __James L. Blank_____________________, Chair, Department of Biological Sciences __John R.D. Stalvey___________________, Dean, College of Arts and Sciences ii TABLE OF CONTENTS Page LIST OF FIGURES ………………………….……………………………………….….xi LIST OF TABLES ……………………………………………………………………...xvi DEDICATION …………………………………………………………………………..xx ACKNOWLEDGEMENTS ………………………………………………………….…xxi CHAPTER I. Introduction ….….………………………………………………………....1 The role of bacteria in aquatic ecosystems ……………………………………………….1 Introduction ……………………………………………………………………….1 The microbial food web …………………………………………………………..2 Bacterial bioenergetics ……………………………………………………………6 Bacterial productivity ……………………………………………………..6 Bacterial respiration ……………………………………………………..10 Bacterial growth efficiency ………...……………………………………11 Phosphorus in aquatic ecosystems ………………………………………………………12 Phosphorus limitation of lake phytoplankton .…………………………………12 The role of bacteria in phosphorus dynamics ………………………………….16 The lability of dissolved organic carbon in aquatic ecosystems ……………………….19 The microbial shunt hypothesis of phosphorus apportionment ………………………..24 Rationale ……………………………………………………………………………….26 iii Introduction to the study site: Lake Erie ………………………………………26 Environmental problems in Lake Erie …………………………………………28 Cultural eutrophication ………………………………………………...28 Non-indigenous species ……………………………………………….31 Hypoxia ………………………………………………………………..33 Causes and consequences ….…………………………………..33 History of hypoxia in Lake Erie: past and present ……………35 Statement of the purpose of this research ……………………………………………...38 Dissertation objectives …………………………………………………………………39 Summary of dissertation findings ……………………………………………………...41 CHAPTER II. Distribution and apportionment of phosphate between bacterioplankton and phytoplankton in Lake Erie………………………………… ………………………44 Abstract ………………………………………………………………………………….44 Introduction ……………………………………………………………………………...45 Methods ………………………………………………………………………………….48 Site characterization ……………………………………………………………..48 Bacterial structure ……………………………………………………………….48 Bacterial productivity ……………………………………………………………49 Plankton phosphorus dynamics ………………………………………………….50 Labile dissolved organic carbon (LDOC) ……………………………………….50 Phosphate uptake ………………………………………………………………..51 Trophic state index (TSI) ….…………………………………………………….52 iv Results …………………………………………………………………………………52 Trophic state index …………….……………………………………………….52 Bacterial structure and productivity ……………………………………………53 Phosphorus dynamics …………………………………………………………..54 Labile dissolved organic carbon ………………………………………………..55 Phosphate apportionment ……………………………………………………….56 Discussion ………………………………………………………………………………56 Acknowledgements ……………………………………………………………………..61 CHAPTER III. Thehe role of LDOC to phosphorus dynamics in Lake Erie bacterioplankton assemblages …………………………………………………………..80 Abstract ………………………………………………………………………………….80 Introduction ……………………………………………………………………..……….82 Methods ………………………………………………………………………..………...86 Sample collection ………………………………………………..………………86 Phosphate uptake and turnover time ……………………………………..……...86 Phosphate apportionment to bacteria and algae …………………………..……..87 Particulate phosphorus and P-quota ………………………………………..……88 Phosphorus distribution to bacteria and algae ………………………………..…89 Biologically available phosphate (BAP) and Michaelis-Menten kinetics …..…..89 Labile dissolved organic carbon (LDOC) …………………………………..…...90 Total dissolved organic carbon (TDOC) ……………………………………..….91 v Testing the microbial shunt hypothesis – Low-molecular weight carbon amendments …………………………………………………...………………………...91 Results …………………………………………………………………..………………91 Limnological variables ……………………………………………………..…...91 LDOC distribution and abundance ………………………………………..…….91 Biologically available phosphate (BAP), phosphate uptake, and turnover time ….………………………………………...…………..………93 Phosphate apportionment to bacteria ………………………………………..…..95 Particulate phosphorus ………………………………………………..…………96 Available phosphorus distribution among bacterioplankton and phytoplankton ………………………………………………………...……..97 Bacterial P-quota ………………………………………………………..……….97 Biologically available phosphate (BAP) and Michaelis-Menten kinetics ……....98 Relationship between LDOC, TSI, and phosphorus dynamics ……………….....99 Relationship between LDOC and bacterial phosphorus dynamics …………….100 Testing the microbial shunt hypothesis – Bacterial response to low molecular weight carbon amendments …………………………………………101 Discussion ……………………………………………………………………………...103 Summary ……………………………………………………………………………….109 Acknowledgements …………………………………………………………………….110 CHAPTER III. Availability of dissolved organic carbon to lake bacterioplankton ……………………………………………………………………..…182 vi Abstract ………………………………………………………………………………...182 Introduction ……………………………...……………………………………………..183 Methods ….……………………………………………………………………………..185 Sample collection ……………………………………………………………...185 Labile dissolved organic carbon (LDOC) …………………………………….186 Total dissolved organic carbon (TDOC) ……………………………………...187 LDOC swap experiments ……………………………………………………..188 Results ………………………………………………………………………………...188 Site characterization …………………………………………………………..188 LDOC distribution………………..…………………………………………...189 Fraction of TDOC that is LDOC ……………………………………………..190 Correlation of LDOC with other variables ...…………….................................191 Variability of LDOC utilization by bacterioplankton ………………………...192 Discussion …………………………………………………………………………….194 Summary ……………………………………………………………………………...198 Acknowledgements ……….…………………………………………………………..199 CHAPTER V. Factors influencing the bioenergetics of Lake Erie bacterioplankton ………………………………………………………………………..241 Abstract ………...………………………………………………………………………241 Introduction ………...…………………………………………………………………..242 Methods ……...…………………………………………………………………………244 vii Sample collection ……..……………………………………………………….244 Bacterial productivity ..………………………………………………………...245 Bacterial respiration …...………………………………………………………245 Bacterial growth efficiency ……………………………………………………246 Bacterial abundance …………………………………………………………...246 Labile dissolved organic carbon (LDOC) ….………………………………….247 Total dissolved organic carbon (TDOC) …….………………………………...247 Particulate phosphorus and P-quota .…………………………………………..248 Chlorophyll a concentration ..………………………………………………….248 Trophic state index (TSI) ..……………………………………………………..249 Results ………………………………………………………………………………...249 Limnological variables ………………………………………………………..249 Bacterial abundance and cellular biovolume …………………………………250 Bacterial productivity (BP) …………………………………………………...251 Bacterial respiration (BR) …………………………………………………….252 Bacterial growth efficiency (BGE) …………………………………………...253 Comparison of vertical profiles …….…………………………………………254 Factors influencing bacterial bioenergetics .…………………………………..256 Discussion …………………………………………………………………………….259 Summary ……………………………………………………………………………...266 Acknowledgements …………….……………………………………………………..267 CHAPTER VI. Life in the dead zone ………………………………………………….307 viii Abstract ………………………………………………………………………………307 Introduction …………………………………………………………………………..309 Methods ………………………………………………………………………...………311 Site characterization ……………………………………………………………311 Bacterial abundance, cellular biovolume, and total biovolume ………………..312 Bacterial productivity …………………………………………………………..312 Bacterial respiration ……………………………………………………………313 Bacterial growth efficiency …………………………………………………….314 Bacterial particulate phosphorus and total phosphorus ………………………..314 Phosphate uptake and total turnover time ……………………………………..315 Microbial loop …………………………………………………………………315 Potential primary productivity …………………………………………………316 Trophic state index (TSI) ………………………………………………………316 Results …………………………………………………………………………………317 Site characterization …………………………………………………………...317 Bacterial assemblage …………………………………………………………..318 Microbial loop …………………………………………………………………318 Bacterial activity ………………………………………………………………319 Phytoplankton activity ………………………………………………………...320 Bacterial phosphorus dynamics ……………………………………………….321 Discussion ……………………………………………………………………………..322 Summary ………………………………………………………………………………322 ix Acknowledgements ……………………………………………………………………347 SUMMARY OF FINDINGS ………….……………………………………………….348 LITERATURE CITED …………………………….…………………………………..357 APPENDIX……………………………………………………………………………..398 x LIST OF FIGURES Page CHAPTER II. Distribution and apportionment of phosphate between bacterioplankton and phytoplankton in Lake Erie Figure 1. Map of Lake Erie with sites labeled …………………………….…………74-75 Figure 2. The relationship between bacterial phosphate uptake and labile dissolved organic carbon…………….……………………………………………………….…76-77 Figure 3. The relationship between P distribution to bacteria (%) and labile dissolved organic carbon (LDOC) concentration (μM) …………………………………….…..78-79 CHAPTER III. The role of LDOC to phosphorus dynamics in Lake Erie bacterioplankton assemblages Figure 1. Map
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