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By Sarah Jaffri the Psychrophilic Green Alga, Chlorella BI Sp. Was

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By Sarah Jaffri the Psychrophilic Green Alga, Chlorella BI Sp. Was ABSTRACT CHARACTERIZATION OF THE PHOTOSYNTHETIC APPARATUS OF CHLORELLA BI SP., AN ANTARCTICA MAT ALGA UNDER VARYING TROPHIC GROWTH STATES by Sarah Jaffri The psychrophilic green alga, Chlorella BI sp. was isolated from a transient Antarctic pond as part of a mat consortium. Previous research on Chlorella BI sp. showed that the organism was able to utilize inorganic and organic forms of carbon and alter its photosynthetic apparatus in response to varying trophic growth states. Based on these early results, the goals of this thesis project were to: (1) characterize the photosynthetic apparatus of Chlorella BI sp. under different trophic states in comparison to the mesophilic species, Chlorella vulgaris; and, (2) determine the effect on the photosynthetic apparatus of Chlorella BI sp, when it is shifted from dark to light conditions. Chlorella BI sp. grew exponentially under the three tested trophic states. The photosynthetic apparatus exhibited functional and structural alteration. It is concluded Chlorella BI sp. has retained the ability to alter its photosynthetic apparatus in response to adaptation to a variable habitat. CHARACTERIZATION OF THE PHOTOSYNTHETIC APPARATUS OF CHLORELLA BI SP., AN ANTARCTICA MAT ALGA UNDER VARYING TROPHIC GROWTH STATES A Thesis Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Master of Science Department of Microbiology by Sarah Jaffri Miami University Oxford, OH 2011 Advisor Rachael Morgan-Kiss Reader D.J. Ferguson Reader Gary R. Janssen TABLE OF CONTENTS Chapter One: Introduction P. 1-11 Chapter Two: Functional and structural Analysis of the different trophic states of Chlorella BI sp. in comparison to the mesohphilic species, Chlorella vulgaris P.12-53 Chapter Three: Alterations in the photosynthetic apparatus of Chlorella BI sp. in response to a mimicked shift from polar winter to summer P.54-67 References P.68-72 ii LIST OF TABLES Table 1: Effect of the addition of various organic carbon sources on the growth of Chlorella BI sp. in the presence or absence of light P. 33 Table 2: Growth kinetics of Chlorella BI sp. in the presence of different trophic conditions P. 35 Table 3: Low temperature (77K) fluorescence emission ratios of Chlorella BI sp. cells grown under different trophic conditions P. 38 Table 4. Steady state Chl a fluorescence parameters of Chlorella BI sp. under the different trophic states P. 40 Table 5: Effect of addition of various organic carbon sources on the growth of C. vulgaris in the presence or absence of light P. 45 Table 6: Growth kinetics of C. vulgaris under the different trophic states P. 46 iii LIST OF FIGURES CHAPTER ONE Figure 1: Transmission Electron micrographs of Chlorella BI sp., P. 9 Figure 2: Photosynthetic apparatus in oxygenic photosynthesis P. 10 Figure 3: Pulse Amplitude Modulation induction curve of Chlorella BI sp. P. 11 CHAPTER TWO Figure 1A: Neighbor joining phylogenetic trees were constructed using the nucleotide sequence of genes rbcL (A) and psbA (B) for Chlorella BI sp. P.32 Figure 2: Growth physiology of Chlorella BI sp. under different trophic conditions. B. Glucose consumption for Chlorella BI sp. under variable trophic growth states P. 34 Figure 3: Chlorophyll a: b ratio and total chlorophyll (ng/cell) for Chlorella BI sp. under variable trophic growth states P. 36 Figure 4: Chl a fluorescence emission spectra at 77K of whole cells of Chlorella BI sp. under the different trophic states states P. 37 Figure 5: Representative room temperature Chl a fluorescence induction curves of whole cells of Chlorella BI sp. grown under variable trophic conditions P. 39 Figure 6: Representative immunoblot of soluble fraction polypeptides isolated from Chlorella BI sp. grown under each trophic state P. 41 Figure 7: Densitometry of Chlorella BI sp. soluble fraction, Rubisco (A) and ferredoxin (B) P. 42 Figure 8A: Representative thylakoid SDS-PAGE gel of Chlorella BI sp., P. 43 Figure 8B: Representative immunoblot of thylakoid polypeptide D1 P. 43 Figure 9: Densitometry of Chlorella BI sp. thylakoid polypeptide, D1 P. 44 Figure 10: Generation time of Chlorella BI sp. compared with C. vulgaris under the different trophic conditions. P. 47 Figure 11: Chlorophyll a: b ratio for C. vulgaris under the different trophic conditions. P.48 Figure 12: Total chlorophyll (ng/cell) for C. vulgaris under the different trophic conditions P. 49 iv Figure 13: Representative room temperature Chl a fluorescence induction curves of whole cells of C. vulgaris grown under variable trophic conditions P. 50 Figure14: Steady state chlorophyll a fluorescence parameters Fv/Fm, qP and qN of C. vulgaris compared to Chlorella BI sp. grown under autotrophic (A), mixotrophic (B) and heterotrophic (C) conditions P. 51 Figure 15: Densitometry of C. vulgaris immunoblots of Rubisco compared to Chlorella BI sp P. 52 Figure 16: Non-denaturing gradient gel for Chlorella BI and C. vulgaris. 2nd dimension gel analysis of the autotrophic states of C. vulgaris (A) and Chlorella BI sp (B) P. 53 CHAPTER THREE Figure 1A: Growth of Chlorella BI sp. during the shift from dark to light P.62 Figure1B: Glucose consumption during the shift from dark to light P.62 Figure 2: Low temperature (77K) fluorescence for Chlorella BI sp. cells shifted from dark to light P.63 Figure 3: Low temperature (77K) emission ratios of Chlorella BI sp. cells shifted from dark to light P.64 Figure 4: Chlorophyll a: b ratios and total chlorophyll (ng/cell) for Chlorella BI sp. during the shift from dark to light P. 65 Figure 5: Steady state Chl a fluorescence trace analysis for Chlorella BI sp. cells shifted from dark to light P. 66 Figure 6: Steady-state chlorophyll fluorescence quenching parameters for Chlorella BI sp. during the shift dark to light P.67 v ACKNOWLEDGMENTS I thank the Department of Microbiology at Miami University and the National Science Foundation (NSF) for supporting this research. I would also like to thank my advisor, Dr. Rachael Morgan-Kiss for her support and guidance throughout this project. To my committee, Dr. Gary Janssen and Dr. D.J. Ferguson, I would like to extend my complete gratitude. I would like to thank my current and former lab mates Jenna Dolhi, Patrick Feasel, Nicholas Ketchum, Scott Bielewicz, Donald Holter, Triratana Sanguanbun, Rocky Patil, Weidong Kong, Audrey Lloyd and Alex Loomis for providing a fun working environment and making our lab a more memorable experience. I thank my parents, Saleem and Ghzala Jaffri, and siblings (Ali, Mariam and Heena) for their constant love and support throughout my Masters. As a family, we have faced a number of uphill battles but that has inevitably made us stronger. I firmly believe that everything we have given up will eventually reap us even bigger rewards. I would also like to thank Dr. Christine Weingart for believing in me as an undergraduate and inspiring me to attend graduate school. Lastly, I would like to thank Zulfiqar Haider for his constant amusement, love and support throughout my time at Miami. vi DEDICATION This thesis is dedicated to my parents, Saleem and Ghzala Jaffri. It is only a small token of appreciation for everything my parents sacrificed to give their children a proper education. For that, we will always be grateful. -Sarah vii CHAPTER ONE INTRODUCTION 1.1 POLAR ENVIRONMENTS About three-fourths of the Earth’s biosphere consists of environments that are exposed to extremely low or permanently frozen temperatures; such habitats include high alpine snowfields, deep oceans, polar sea ice, ice-covered lakes and transitory ponds (Morgan-Kiss, et al., 2006). Permanently cold environments are often dominated by microorganisms such as gram negative and gram positive bacteria, Archaea, yeast, cyanobacteria and algae. These organisms are adapted to not only surviving but thriving in cold ecosystems (Morgan-Kiss, et al., 2006). 1.2 EXTREME ENVIRONMENTS Extreme environments are considered inhospitable for most life forms because of conditions such as high temperature, ionizing radiation, pressure, low nutrients and varying pH (Rothchild and Mancinelli, 2001). Low temperature environments are examples of one extreme habitat; however, despite permanent cold, these environments vary greatly in their chemical and physical properties, influencing the survival strategies of organisms in such habitats (Morgan-Kiss, et al., 2006; Neale and Priscu, 1995). It is important to determine how organisms are able to adapt and survive to such ecosystems because it will provide insight into one of the most prevalent types of habitats in the world which are being significantly impacted by climate change (Morgan-Kiss, et al., 2006). Many cold-adapted microorganisms residing in polar habitats are psychrophilic (i.e. optimal temperature < 15°C) (Morita, 1975). Photopsychrophiles are a class of psychrophiles that are able to fix carbon by using light energy and require low temperatures for growth (Morgan-Kiss, et al., 2006). These organisms have been isolated from varying permanently cold environments such as microbial mats (Hawes and Howard-Williams, 2003), the underside of sea ice, and within the water column of 1 permanently ice-capped lakes. Like all photosynthetic organisms, photopsychrophiles use the photochemical apparatus to convert light energy into chemically-stored energy products which are ultimately used to fix inorganic carbon. 1.3 MICROBIAL MATS IN POLAR ENVIRONMENTS Microbial mats are abundant in polar environments and consist of stratified organically rich layers of microbes found on the surfaces of rocks, soil or aquatic sediment (De los Rios, et al., 2004). They are dominated by cyanobacteria and other photosynthetic organisms, which form a biological refuge for a diverse collection of other heterotrophic and chemotrophic microorganisms (Ramsing, et al., 1993; Risatti, et al., 1994). Microbial mats are vertically stratified at the level of biology and physical features (light, nutrients, redox potentials, oxygen)(Paerl and Pinckney, 1996) . Primary producers reside on the mat surface, which is considered the oxic zone of the mat, contributing to primary production and nutrient cycling in the mat.
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