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UNIVERSITY of CALIFORNIA, SAN DIEGO the Genus Salinispora As A UNIVERSITY OF CALIFORNIA, SAN DIEGO The genus Salinispora as a model organism for species concepts and natural products discovery A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Marine Biology by Natalie Millán Aguiñaga Committee in charge: Paul R. Jensen, Chair Eric E. Allen William Fenical Joseph Pogliano Gregory W. Rouse 2016 Copyright Natalie Millán Aguiñaga, 2016 All rights reserved The dissertation of Natalie Millán Aguiñaga is approved, and it is acceptable in quality and form for publication on microfilm and electronically: __________________________________________________________________ __________________________________________________________________ __________________________________________________________________ __________________________________________________________________ __________________________________________________________________ Chair University of California, San Diego 2016 iii DEDICATION To my parents Roberto and Yolanda. Thanks for sharing this dream come true and for continuing to support me in the dreams I still want to achieve. iv TABLE OF CONTENTS Signature Page ...................................................................................................... iii Dedication ............................................................................................................. iv Table of Contents ................................................................................................ v List of Figures ...................................................................................................... vii List of Tables ....................................................................................................... ix Acknowledgments ................................................................................................. x Vita ...................................................................................................................... xiv Abstract of the Dissertation .................................................................................. xvi Chapter 1 Introduction .................................................................................. 1 1.1. Overview of the dissertation .......................................................... 2 1.2. Bacterial species concepts: pre- and post-genomic era ................ 4 1.3. Actinomycetes and their potential for natural products ................ 12 1.4. Molecular targets .......................................................................... 15 1.5. Salinispora as a model organism .................................................. 17 1.6. References ...................................................................................... 19 Chapter 2 Multilocus sequence typing reveals evidence of homologous recombination linked to antibiotic resistance in the genus Salinispora ...................................................................................... 26 2.1. Abstract .......................................................................................... 27 2.2. Introduction ................................................................................... 28 2.3. Material and methods ..................................................................... 32 2.4. Results ........................................................................................... 38 2.5. Discussion ..................................................................................... 43 2.6. References ..................................................................................... 46 Chapter 3 Phylogenomic analyses and species delineations within the genus Salinispora ...................................................................................... 51 3.1. Abstract ......................................................................................... 52 3.2. Introduction ................................................................................... 53 v 3.3. Material and methods ..................................................................... 57 3.4. Results ........................................................................................... 62 3.5. Discussion ..................................................................................... 83 3.6. References ..................................................................................... 88 Chapter 4 Comparative genomics as a method to identify resistance genes in biosynthetic gene clusters ............................................................... 93 4.1. Abstract ....................................................................................... 94 4.2. Introduction ................................................................................. 94 4.3. Material and methods ..................................................................... 98 4.4. Results ......................................................................................... 100 4.5. Discussion ................................................................................... 112 4.6. References ................................................................................... 116 Chapter 5 Concluding remarks ....................................................................... 121 5.1. References ..................................................................................... 127 Appendix A Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora ................................................ 130 Appendix B CRISPR-Cas systems in the marine actinomycete Salinispora: linkages with phage defense, microdiversity and biogeography.. 142 vi LIST OF FIGURES Chapter 2 Figure 2.1. Collection sites and number of strains sequenced ............................. 36 Figure 2.2. The rpoB gene ................................................................................... 36 Figure 2.3. Concatenated neighbor-joining phylogeny from the 16S RNA, atpD, 41 gyrB, trpB, recA and rpoB(3) loci (3,330 bp.) ..................................................... Figure 2.4. Neighbor-joining phylogenetic tree based on 188 aa from rpoB(2) .... 42 Chapter 3 Figure 3.1. Geographic origins of strains ............................................................ 68 Figure 3.2. Core orthologous groups rarefaction curves ................................... 72 Figure 3.3. Rarefaction curves for the total number of orthologous groups ......... 72 Figure 3.4. Orthologous groups distribution in Salinispora spp. ...................... 73 Figure 3.5. Salinispora maximum likelihood phylogeny (concatenated) based on all shared single-copy genes, genes not under recombination and genes under recombination ........................................................................................................ 74 Figure 3.6. ASTRAL species tree phylogeny based on all the shared single-copy genes, genes not under recombination and genes under recombination ............. 75 Figure 3.7. Comparison of the concatenated tree using the genes not under recombination and the ASTRAL species tree using the same data ........................ 76 Figure 3.8. Average Nucleotide Identity (ANI) dendrogram for 119 Salinispora strains .................................................................................................................... 77 Figure 3.9. Average Nucleotide Identity and Alignment Fraction (ANI-AF) .... 78 Figure 3.10. Average Nucleotide Identity and Alignment Fraction (ANI-AF) networks based on the location of the strains ...................................................... 79 Figure 3.11. Circular phylogenetic tree derived from the concatenation of all the single-copy shared genes not under recombination and the ANI-AF networks .... 80 vii Figure 3.12. Comparison of the S. pacifica species tree with secondary metabolite gene clusters distribution, based on the presence/absence of predicted biosynthetic gene clusters ..................................................................................... 81 Figure 3.13. Comparison of the S. pacifica species tree with the matrix of gene content of the COG category of energy production and conversion [C] ............. 82 Chapter 4 Figure 4.1. Bioinformatic identification of candidate resistance genes .............. 104 Figure 4.2. Phylogenetic tree of the 12 duplicated orthologous groups of FabF/B homologous in comparison with the platensimycin (Ptm) and platencin (Ptn) ....... 109 Figure 4.3. Comparison of the tlm locus in six Salinispora strains and their position in the Salinispora species phylogenetic tree ........................................ 110 Figure 4.4. Likelihood reconstruction showing the distribution of the orthologous group Salin8269 that is related with the resistance gene in the Salinispora phylogeny .......................................................................................... 111 viii LIST OF TABLES Chapter 2 Table 2.1. List of PCR primers and conditions .................................................. 37 Table 2.2. Population parameters calculated using nucleotide sequences ........... 40 Table 2.3. Regions 1 and 2 of the translated rpoB gene ......................................... 40 Chapter 3 Table 3.1. Distribution of clusters of orthologous groups (COGs) based on major functional gene categories .................................................................................. 61 Table 3.2. General characteristics of the 119 Salinispora strains ........................
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