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Download The COPPER NUTRITION AND TRANSPORT MECHANISMS IN PLANKTON COMMUNITIES IN THE NORTHEAST PACIFIC OCEAN by David Mathew Semeniuk B.Sc., The University of British Columbia, 2006 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Oceanography) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) October 2014 © David Mathew Semeniuk, 2014 Abstract Copper (Cu) is an essential micronutrient for phytoplankton, particularly during iron limitation, but can also be toxic at relatively low concentrations. While Cu stoichiometry and metabolic functions in marine phytoplankton have been studied, little is known about the substrates for Cu transport and the Cu nutritional state of indigenous phytoplankton communities. The aim of my thesis was two-fold: investigate the bioavailability of organically bound Cu to laboratory and indigenous phytoplankton, and evaluate Cu nutrition of phytoplankton along Line P, a coastal- open ocean transect in the northeast subarctic Pacific Ocean. Organically complexed Cu was bioavailable to four laboratory phytoplankton strains and an Fe-limited phytoplankton community. A laboratory investigation of the substrates for the high-affinity Cu transport system in the model diatom Thalassiosira pseudonana confirmed that organically complexed Cu(II) can be acquired, and likely via extracellular reduction and internalization of Cu(I). Cellular uptake rates of the laboratory strains were similar to those estimated for the natural phytoplankton assemblage, and provide additional evidence that some in situ Cu ligand complexes are likely bioavailable. Using bottle incubations, I investigated the potential for Cu limitation and toxicity in open ocean Fe-limited phytoplankton communities. In 2010, I provided physiological evidence for an interaction between Fe and Cu metabolisms in an Fe-limited phytoplankton community. In 2011, Cu availability to an Fe-limited community was reduced, using a strong Cu(II)-specific ligand, resulting in slower Cu uptake rates, faster growth rates, and increased cyanobacteria abundance. Despite large variations in macronutrient, light, and iron along Line P in 2011, net primary productivity was negatively correlated with inorganic Cu concentrations, and positively correlated with the strength of the in situ ligands. The potential roles of Cu ii ligands in the sea are discussed, highlighting that the bioavailability of in situ organic Cu complexes is a key determinant for marine primary productivity. iii Preface A version of Chapter 2 is currently under review for publication: D. M. Semeniuk, R. M. Bundy, C. D. Payne, K. A. Barbeau, and M. T. Maldonado, (accepted with revisions). Acquisition of organically complexed copper by marine phytoplankton and bacteria in the NE subarctic Pacific Ocean. I designed the experiment, executed the majority of the field sampling and sample analysis, performed the majority of the data analysis, and wrote the manuscript. C. D. Payne assisted in field sampling. R. M. Bundy measured the ligand conditional stability constants, and measured the total dissolved Cu sample. Dr. K. A. Barbeau and Dr. M. T. Maldonado provided editorial assistance and invaluable feedback on data analysis during preparation of the manuscript. A version of Chapter 3 is currently in preparation for submission to a scientific journal. The co- authors are: D. M. Semeniuk and M. T. Maldonado. Title: Acquisition of organically complexed Cu(II) by a high-affinity Cu transport system in marine phytoplankton. I designed and executed the experiment, and wrote the manuscript. Dr. M. T. Maldonado provided editorial assistance during preparation of the manuscript. A version of Chapter 4 is currently in preparation for submission to a scientific journal. The co- authors are: D.M. Semeniuk, R. L. Taylor, R. M. Bundy, W. K. Johnson, J. T. Cullen, K. A. Barbeau, and M. T. Maldonado. Title: Iron-copper interactions in HNLC phytoplankton in the northeast subarctic Pacific Ocean. I designed the incubation experiments, executed the majority of the field sampling and sample analysis, performed the majority of the data analysis, and wrote iv the manuscript. R. L. Taylor assisted in field sampling, and R. M. Bundy measured the copper speciation sample. W. K. Johnson assisted with field sampling and measured the dissolved Fe samples, and M. Robert organized the field expedition and provided ancillary data. Dr. J. T. Cullen provided expertise and instrumentation to make the dissolved Cu measurements. Dr. K. A. Barbeau and Dr. M. T. Maldonado provided editorial assistance and feedback on data analysis during preparation of the manuscript. A version of Chapter 5 is currently in preparation for submission to a scientific journal. The co- authors are: D.M. Semeniuk, A. Posacka, R. M. Bundy, M. Robert, K. A. Barbeau, and M. T. Maldonado. Title: The effects of copper speciation on phytoplankton and bacterial rate processes in the northeast subarctic Pacific Ocean. I designed the incubation experiment and transect sampling plan. I performed all of the radioisotope work, and a large portion of the sample collection and processing. A. Posacka assisted with transect and incubation sampling, R. M. Bundy measured the copper speciation samples, and M. Robert provided ancillary data and organized the field expedition. Dr. K. A. Barbeau and Dr. M. T. Maldonado assisted with data interpretation and provided editorial feedback during the preparation of the manuscript. v Table of Contents Abstract.......................................................................................................................................... ii! Preface........................................................................................................................................... iv! Table of Contents ......................................................................................................................... vi! List of Tables .............................................................................................................................. xiv! List of Figures............................................................................................................................. xix! Acknowledgements ....................................................................................................................xxv! Dedication ................................................................................................................................ xxvii! Chapter 1: Introduction ................................................................................................................1! 1.1! Trace Metal Control of Primary Productivity.................................................................... 3! 1.1.1! Trace Metal Speciation and Notation ......................................................................... 3! 1.1.2! Trace Metal Bioavailability to Marine Phytoplankton ............................................... 5! 1.1.3! Case Study of Trace Metal Limitation – Iron ............................................................. 9! 1.1.4! Trace Metal Toxicity................................................................................................. 11! 1.2! Copper Physiology in Marine Phytoplankton.................................................................. 13! 1.2.1! Phytoplankton Metabolic Copper Requirements and Homeostasis.......................... 13! 1.2.2! Copper Detoxification............................................................................................... 15! 1.2.3! The Distribution and Speciation of Copper in Seawater .......................................... 16! 1.2.4! Copper Bioavailability and Transporter Substrates .................................................. 20! 1.2.5! Copper Nutritional Status of Natural Marine Phytoplankton Populations ............... 23! 1.3! Oceanography of the Northeast Subarctic Pacific Ocean................................................ 24! 1.3.1! Water Properties and Circulation.............................................................................. 25! vi 1.3.2! Phytoplankton and Nutrient Dynamics along Line P ............................................... 26! 1.3.3! Copper Concentration and Speciation along Line P................................................. 27! 1.4! Thesis Organization ......................................................................................................... 27! 1.5! Figures.............................................................................................................................. 33! Chapter 2: Acquisition of Organically Complexed Copper by Marine Phytoplankton and Bacteria in the NE Subarctic Pacific Ocean..............................................................................37! 2.1! Introduction...................................................................................................................... 38! 2.2! Materials and Methods..................................................................................................... 41! 2.2.1! Sampling and Incubation .......................................................................................... 41! 2.2.2! Determination of Initial Chemical and Biological Parameters................................. 42! 2.2.3! Determination of Conditional Stability Constants for Cyclam and Cyclen.............. 43! 2.2.4! Preparation of the Copper-Ligand Complex Additions for Copper Uptake
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