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UNDERSTANDING the GENOMIC BASIS of STRESS ADAPTATION in PICOCHLORUM GREEN ALGAE by FATIMA FOFLONKER a Dissertation Submitted To

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UNDERSTANDING the GENOMIC BASIS of STRESS ADAPTATION in PICOCHLORUM GREEN ALGAE by FATIMA FOFLONKER a Dissertation Submitted To UNDERSTANDING THE GENOMIC BASIS OF STRESS ADAPTATION IN PICOCHLORUM GREEN ALGAE By FATIMA FOFLONKER A dissertation submitted to the School of Graduate Studies Rutgers, The State University of New Jersey In partial fulfillment of the requirements For the degree of Doctor of Philosophy Graduate Program in Microbial Biology Written under the direction of Debashish Bhattacharya And approved by _________________________________________________ _________________________________________________ _________________________________________________ _________________________________________________ New Brunswick, New Jersey January 2018 ABSTRACT OF THE DISSERTATION Understanding the Genomic Basis of Stress Adaptation in Picochlorum Green Algae by FATIMA FOFLONKER Dissertation Director: Debashish Bhattacharya Gaining a better understanding of adaptive evolution has become increasingly important to predict the responses of important primary producers in the environment to climate-change driven environmental fluctuations. In my doctoral research, the genomes from four taxa of a naturally robust green algal lineage, Picochlorum (Chlorophyta, Trebouxiphycae) were sequenced to allow a comparative genomic and transcriptomic analysis. The over-arching goal of this work was to investigate environmental adaptations and the origin of haltolerance. Found in environments ranging from brackish estuaries to hypersaline terrestrial environments, this lineage is tolerant of a wide range of fluctuating salinities, light intensities, temperatures, and has a robust photosystem II. The small, reduced diploid genomes (13.4-15.1Mbp) of Picochlorum, indicative of genome specialization to extreme environments, has resulted in an interesting genomic organization, including the clustering of genes in the same biochemical pathway and coregulated genes. Coregulation of co-localized genes in “gene neighborhoods” is more prominent soon after exposure to salinity shock, suggesting a role in the rapid response to salinity stress in Picochlorum. Despite the pressure for genome reduction, key gene gains are seen through gene family expansion of an important ii SOS1 salt transporter and through bacterium-derived horizontal gene transfer (HGT). Thirteen instance of HGT were identified that display differential acquisition among Picochlorum taxa, indicating an ongoing process in this lineage. The presence of introns, differential expression under salinity shock, and the use of high quality genomes from closely related species provide robust support for the integration of HGT candidates into host nuclear genomes. Transferred genes are potentially functionally relevant and include encoded proteins with roles related to osmolyte production, cell wall metabolism, and metabolic flexibility. A transcriptomic comparison of two sister taxa with very similar genomes, Picochlorum SENEW3 from a brackish lagoon and Picochlorum oklahomensis from a hypersaline salt plain environment was performed under high (1.5 M NaCl) and low salinity (10mM NaCl) shock conditions. This work revealed different regulation responses to salinity shock in terms of osmolyte production, reflecting nitrogen availability in the respective environments, and indicating that the habitat-driven regulation of the existing gene inventory is key to environmental adaptation. These diploid sister taxa also reveal one striking difference between them, levels of haplotype heterozygosity. RNA-seq expression data supports condition-dependent allele-specific gene expression, indicating a functional relevance to maintaining a large divergent allele pool in P. oklahomensis. Overall, Picochlorum has revealed differences in adaptation strategies between seemingly identical species with regard to morphology and gene sequence similarity. My study has provided insights into the adaptive strategies used by eukaryotes with reduced gene inventories that is reflected in selection acting on genome organization, gene regulation, and specialization. iii ACKNOWLEDGMENTS I would like to thank my advisor, Dr. Debashish Bhattacharya, for his guidance, patience, and support; my committee members Dr. Kay Bidle, Dr. Jeff Boyd, and Dr. Lena Struwe; the Microbial Biology graduate program director, Dr. Gerben Zylstra; research collaborators, Dr. G. C. Dismukes, Dr. Gennady Ananyev, Dr. Hwan Su Yoon, and Dr. Mehdi Javinmard; the members of the Bhattacharya lab for their advice and help, my mom and dad for supporting me and my education, and my family and friends for their support. I would also like to thank Dr. H. Boyd Woodruff for the fellowship support for the first year in the Microbial Biology graduate program, The Phycological Society of America for research support, and the NSF-IGERT (Integrative Graduate Education Research Traineeship) for renewable fuels at Rutgers University (0903675) for fellowship support. iv DEDICATION To the memory of my late husband, Mahmood. v ACKNOWLEDGEMENT OF PUBLICATIONS Chapter 2 has been published as Foflonker F, Price DC, Qiu H, Palenik B, Wang S & Bhattacharya D (2015) Genome of the halotolerant green alga Picochlorum sp. reveals strategies for thriving under fluctuating environmental conditions. Environ Microbiol 17: 412-426. F. Foflonker participated in writing the manuscript and is directly responsible for all genomic analyses and figures 2-7 and all tables. Chapter 3 has been published as Foflonker F, Ananyev G, Qiu H, Morrison A, Palenik B, Dismukes GC & Bhattacharya D (2016) The unexpected extremophile: Tolerance to fluctuating salinity in the green alga Picochlorum. Algal Research 16: 465-472. F. Foflonker participated in writing the manuscript and is directly responsible for all analyses, tables, and figures. Chapter 4 is being prepared for publication as Foflonker F, Mollegard D, Ong M, Yoon HS, & Bhattacharya D (2018). Genomic anlysis of Picochlorum species reveals how microalgae adapt to fluctuating environments. F. Foflonker participated in writing the manuscript and is directly responsible for all analyses, tables, and figures. vi TABLE OF CONTENTS Abstract of the Dissertation ............................................................................................ ii Acknowledgments .......................................................................................................... iv Dedication ....................................................................................................................... v Acknowledgement of Publications ................................................................................ vi Table of Contents .......................................................................................................... vii List of Tables ................................................................................................................. xi List of Figures .............................................................................................................. xiv Chapter 1: Introduction ................................................................................................... 1 Microalgae as biofuel feedstock ................................................................................. 1 Salinity stress on eukaryotic microalgae .................................................................... 3 Picochlorum as a biofuel candidate and model to study salinity stress ..................... 7 Scope of the thesis ....................................................................................................... 9 Chapter 2: Genome of the haloterant green alga Picochlorum sp. reveals strategies for thriving under fluctuation environmental conditions .................................................... 11 Abstract ..................................................................................................................... 11 Introduction ............................................................................................................... 12 Results ....................................................................................................................... 13 Genome features and phylogeny ........................................................................... 13 Clusters of functionally related genes ................................................................... 14 Transporter analysis .............................................................................................. 17 Growth rates in the presence of organic carbon sources ....................................... 20 HGT analysis ........................................................................................................ 21 vii Selenoproteins ....................................................................................................... 24 Hydrogenase activity and other genes of interest ................................................. 25 Discussion ................................................................................................................. 25 Experimental Procedures .......................................................................................... 27 Strains and culture conditions ............................................................................... 27 DNA and RNA extraction and library construction ............................................. 28 Genome and transcriptome sequencing ................................................................ 28 Construction of multi-protein tree ........................................................................ 29 Phylogenomic
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