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S Ignature Redacted Exploring the Effects of Proteorhodopsin on the Physiology of Native and Heterologous Hosts by Michael Valliere Bachelor of Science, Biochemistry and Molecular Biology Bachelor of Business Administration, Business Management University of Massachusetts Amherst, 2009 Submitted to the Department of Civil and Environmental Engineering in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Environmental Biology MASSACFWMT1S INSTffUTE OF TECHNOLOGY at the SEP 216 MASSACHUSETTS INSTITUTE OF TECHNOLOGY LIBRARIES September 2016 ARQHIVES 0 2016 Massachusetts Institute of Technology. All Rights Reserved. Signature of Author: S ignature redacted Michael Valliere Department of Civil and Environmental Engineering Certified Signature redacted Edward F. DeLong Department of Civil and Envirt al Engineering and Biological Engineering Accepted by: Signature redacted I Jesse Kroll Professor of Civil and Environmental Engineering Chair, Graduate Program Committee Exploring the Effects of Proteorhodopsin on the Physiology of Native and Heterologous Hosts by Michael Valliere Submitted to the Department of Civil and Environmental Engineering on August 18, 2016 in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Environmental Biology ABSTRACT Photoheterotrophic microbes use proteorhodopsin (PR) and other types of microbial rhodopsin photosystems to harness energy directly from sunlight. This thesis explores the photophysiology of PR in the context of a natural marine isolate, Dokdonia sp. strain MED 134, and by establishing Escherichiacoli as a heterologous host to experimentally determine conditions under which the PR photosystem is capable of enhancing growth rate and yield. In Dokdonia sp. MED 134, PR and 11 other genes were discovered to be significantly induced by light but the induction of these genes increased growth rate and yield in an extremely carbon-limited environment; in richer media the induction of the genes by light had an inhibitory effect on growth. In E. coli, various genetic backgrounds were tested with PR expression, and one was discovered to exhibit slightly higher cell yields presumably as a result of light-driven proton pumping by PR. This work illustrates that PR is part of orchestrated response to light in a PR-containing isolate, but can also influence the growth of a heterologous host on its own. Further refinement of the genetic background of E. coli should unlock the full potential of PR as a cellular energy source for biotechnological applications-at least within this organism. Thesis Supervisor: Edward F. DeLong Title: Professor 3 Table of Contents Chapter 1. The Ecological and Physiological Significance of Proteorhodopsin (PR) Biological light energy capture............................................................................ 9 Photosynthesis........................................................................................ 9 Rhodopsin photosystens........................................................................... I Rhodopsin photosystems fill the gap in PA R........................................ 13 M icrobial rhodopsin photosystem s.................................................................... 15 Discovery of ion pum ping rhodopsin photosystem s.............................. 18 Geography and diversity of PR photosysterns........................................ 19 Physiological effects associated with PR photosystem s........................................ Natural isolates......................................................................................24 Heterologous hosts.....................................................................................25 Engineered system s............................................................................... 32 Other form s of ion pumping rhodopsin photosystem s....................................... 35 Photoheterotrophic metabolism and the carbon cycle....................................... 38 Thesis overview................................................................................................. 41 Chapter I. The Physiological Effects of Proteorhodopsin in Flavobacteria A b stra ct..................................................................................................................4 3 Introduction..................................................................................................... 45 M e th o d s..................................................................................................................4 7 Growth experim ents............................................................................... 47 RNA-seq............................................................................................... 48 R e su lts.................................................................................................................... 5 1 Growth of MED1 34 at low and high DOC concentrations....................51 Light induced gene expression in M ED 134.......................................... 53 Differential gene expression during late exponential phase (low DOC) ... 56 Differential gene expression during stationary phase (high DOC)........57 D isc u ssio n .............................................................................................................. 5 9 Light induced gene expression in M ED 134.......................................... 59 5 Transporter expression in low DOC cultures.........................................64 The influence of beta-oxidation in high DOC media.............................66 The ecophysiological impact of PR photosystems................................68 Chapter III. The Physiological Effects of Proteorhodopsin in Escherichia coli A b stra ct..................................................................................................................7 1 Intro d uctio n ............................................................................................................ 7 3 Escherichiacoli as a heterologous host for PR gene expression...........74 Influence of the genetic background on respiration...............................75 Influence of the genetic background on membrane properties..............77 Influence of the genetic background on acetate production..................79 M eth od s.................................................................................................................. 8 0 Bacterial strains and plasm ids................................................................ 80 G row th Experim ents............................................................................. 81 R esults and D iscussion...................................................................................... 83 PR expression in wild-type backgrounds.............................................. 83 PR expression in gene knockout backgrounds.......................................89 The effects ofvidc, atpAGD, and nox on BW25 113 and ApykF...........89 The effects of yidc, pyc, and keJFC* on AfadR.....................................95 C o nc lu sio n s..........................................................................................................10 6 Future optim ization experim ents.............................................................107 Future applications of PR and ion pumping rhodopsin photosystems.....110 Chapter IV. Conclusions and Future Directions for Research.........................................113 Light-enhanced growth in natural PR-containing flavobacateria........................ 115 Engineering E. coli for light enhanced-growth with PR...................................... 119 Appling results from MED 134 to engineer E. coli..............................................124 Engineering the genetic background with serial transfer evolution.....................126 Future applications of PR and other ion-pumping photosystems........................129 6 Chapter V . References................................................................................................. 13 1 Chapter VI. Appendix......................................................................................................147 Supplem entary M aterials for Chapter 11..............................................................147 Supplem entary M aterials for Chapter 111.......................................................... 155 7 I. The Ecological and Physiological Significance of Proteorhodopsin Biological light energy capture Sunlight is-and always has been-an essential resource for life on Earth. The constant bombardment of sunlight energized the abiotic Earth long before life existed, and along with geothermal processes, catalyzed the formation of the reduced chemicals that served as electron donors to the first life forms. Hundreds of millions of years later, evolved versions of these early life forms gained the ability to directly harness the energy within sunlight by converting it to useful cellular energy, and this capability set Earth and its inhabitants on the trajectory that has given rise to the planet we experience today. Photosynthesis In its present form, life on Earth has invented and refined only two distinct systems for light mediated biochemical energy capture (Bryant and Frigaard, 2006). Chlorophyll- based photosynthesis is the better-known system, leveraged by organisms ranging from microscopic cyanobacteria to large multicellular plants. The many different forms of chlorophyll-based photosynthetic systems all work by exciting electrons
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