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University of California Santa Cruz UNIVERSITY OF CALIFORNIA SANTA CRUZ ECOLOGY AND EVOLUTION OF DIATOM-ASSOCIATED CYANOBACTERIA THROUGH GENETIC ANALYSES A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in OCEAN SCIENCES by Jason A. Hilton June 2014 The Dissertation of Jason A. Hilton is approved: Professor Jonathan Zehr, chair Professor Raphael Kudela Professor Jack Meeks Professor Tracy Villareal Tyrus Miller Vice Provost and Dean of Graduate Studies Copyright © by Jason A. Hilton 2014 Table of Contents Title Page ___________________________________________________________ i Table of Contents ___________________________________________________ iii List of Tables and Figures ____________________________________________ vi Abstract __________________________________________________________ viii Acknowledgements __________________________________________________ x Introduction ________________________________________________________ 1 Oceanic N2 fixation _________________________________________________ 1 Heterocyst-forming cyanobacteria in symbiosis ___________________________ 2 Three common DDAs _______________________________________________ 4 DDA global distribution and significance ________________________________ 7 The metabolism of diatom symbionts __________________________________ 10 Interruption elements in heterocyst-forming cyanobacteria _________________ 12 Chapter 1: Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont ______________________________________ 14 Abstract _________________________________________________________ 15 Introduction ______________________________________________________ 15 Methods _________________________________________________________ 17 H. hauckii and H. membranaceus symbiont DNA preparation _____________ 17 H. hauckii and H. membranaceus symbiont genome assembly ____________ 19 CalSC DNA preparation __________________________________________ 20 CalSC genome assembly __________________________________________ 20 Genomic analysis ________________________________________________ 21 Results __________________________________________________________ 22 General features of the diatom symbiont genomes ______________________ 22 Nitrogen metabolism of the diatom symbionts _________________________ 23 iii Gene interruptions on the diatom symbiont nif operon ___________________ 25 Discussion _______________________________________________________ 26 Conclusions ______________________________________________________ 30 Acknowledgements ________________________________________________ 30 Tables and Figures ________________________________________________ 32 Chapter 2: The genomic sequence of the Rhizosolenia clevei symbiont and comparison with other diatom symbionts ______________________________ 44 Abstract _________________________________________________________ 45 Introduction ______________________________________________________ 45 Methods _________________________________________________________ 48 Sample collection and DNA preparation ______________________________ 48 Genome assembly _______________________________________________ 50 Genomic analysis ________________________________________________ 51 Results and Discussion _____________________________________________ 51 Genome characteristics ___________________________________________ 51 Nitrogen metabolism _____________________________________________ 52 Additional unique DDA gene presence/absence ________________________ 55 Conclusions ______________________________________________________ 59 Acknowledgements ________________________________________________ 59 Tables and Figures ________________________________________________ 60 Chapter 3: Metatranscriptomics of N2-fixing cyanobacteria in the Amazon River plume ____________________________________________________________ 65 Abstract _________________________________________________________ 66 Introduction ______________________________________________________ 67 Materials and methods _____________________________________________ 69 Sample collection _______________________________________________ 69 Sample preparation for DNA sequencing _____________________________ 70 Sample preparation for total community RNA _________________________ 71 Sample preparation for poly(A)-tail-selected RNA ______________________ 72 Internal Standards _______________________________________________ 72 iv Sequencing and post-sequencing screening ___________________________ 73 Identification and analysis of diazotroph reads _________________________ 74 Results __________________________________________________________ 75 Environmental sequence similarity to references _______________________ 76 Diazotroph metagenomes _________________________________________ 77 Diazotroph transcriptomes _________________________________________ 78 Discussion _______________________________________________________ 82 Conclusions ______________________________________________________ 90 Acknowledgements ________________________________________________ 91 Tables and Figures ________________________________________________ 92 Chapter 4: Distribution and diversity of DNA elements within functional genes of heterocyst-forming cyanobacteria__________________________________ 104 Abstract ________________________________________________________ 105 Introduction _____________________________________________________ 105 Materials and Methods ____________________________________________ 106 Results _________________________________________________________ 110 Discussion ______________________________________________________ 115 Interrupted genes _______________________________________________ 116 Evolution of elements ___________________________________________ 119 Element gene content ____________________________________________ 121 Conclusions _____________________________________________________ 123 Acknowledgements _______________________________________________ 124 Tables and Figures _______________________________________________ 125 Conclusions ______________________________________________________ 138 References _______________________________________________________ 141 v List of Tables and Figures Chapter 1: Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont Table 1. Nostocales genomes. __________________________________________ 32 Table 2. Genes of obligate symbionts. ___________________________________ 33 Figure 1. Diatom-diazotroph association images.___________________________ 34 Figure 2. Hemiaulus hauckii symbionts on the flow cytometer. _______________ 35 Figure 3. Richelia intracellularis HH01 contig lengths.______________________ 36 Figure 4. Calothrix rhizosoleniae SC01 contigs. ___________________________ 37 Figure 5. Nostocales phylogeny. ________________________________________ 38 Figure 6. Gene similarity of Hemiaulus spp. symbionts. _____________________ 39 Figure 7. Richelia intracellularis HH01 nitrogen metabolism pathway. _________ 40 Figure 8. Nitrogen metabolism genes throughout closed genomes. _____________ 41 Figure 9. GOGAT remnants in Richelia intracellularis HH01. ________________ 42 Figure 10. The Richelia intracellularis HH01 nifH element. __________________ 43 Chapter 2: The genomic sequence of the Rhizosolenia clevei symbiont and comparison with other diatom symbionts Table 1. Nostocales genome statistics. ___________________________________ 60 Table 2. Nitrogen metabolism genes in three diatom symbiont genomes. ________ 61 Figure 1. Richelia in association with Rhizosolenia. ________________________ 62 Figure 2. Richelia intracellularis RC01.__________________________________ 63 Figure 3. Nitrogen metabolism pathways of diatom symbionts. _______________ 64 Chapter 3: Metatranscriptomics of N2-fixing cyanobacteria in the Amazon River plume Table 1. Sample info and sequencing statistics for the Amazon River plume samples. __________________________________________________________________ 92 Table 2. Oceanic cyanobacterial diazotroph genomes. _______________________ 93 Table 3. Trichodesmium hetR sequences in the Amazon River plume. __________ 94 Figure 1. Stations sampled in the Amazon River plume. _____________________ 95 vi Figure 2. Similarity of Amazon River plume diazotroph populations to reference genomes. __________________________________________________________ 96 Figure 3. Similarity of Amazon River plume Trichodesmium populations to other Trichodesmium sequences. ____________________________________________ 97 Figure 4. Diazotroph DNA and cDNA abundances. _________________________ 98 Figure 5. cDNA read coverage on abundant diazotroph transcripts. ____________ 99 Figure 6. HR-B population nitrogenase transcripts. ________________________ 100 Figure 7. Diazotroph categorized transcription. ___________________________ 101 Figure 8. Diazotroph energy metabolism transcription. _____________________ 102 Figure 9. Diazotroph photosynthesis transcription. ________________________ 103 Chapter 4: Distribution and diversity of DNA elements within functional genes of heterocyst-forming cyanobacteria Table 1. Genes interrupted by elements. _________________________________ 125 Table 2. Interruption elements. ________________________________________ 126 Figure 1. Element excision cartoon. ____________________________________ 128 Figure 2. Heterocyst-forming cyanobacteria 16S phylogeny. ________________ 129 Figure 3. Serine recombinase phylogeny with element lengths. ______________ 130 Figure
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