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Population Dynamics and Metabolic Potential of a Pilot-Scale Microbial Community Population dynamics and metabolic potential of a pilot-scale microbial community performing enhanced biological phosphorus removal by CHRISTOPHER EVAN LAWSON B.A.Sc. (Civil Engineering), University of British Columbia, 2010 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF APPLIED SCIENCE in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Civil Engineering) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) September 2014 © Christopher Evan Lawson, 2014 Abstract Enhanced biological phosphorus removal (EBPR) is an environmental biotechnology of global importance, essential for protecting receiving waters from eutrophication and enabling phosphorus recovery. Current understanding of EBPR is largely based on empirical evidence and black-box models that fail to appreciate the driving force responsible for nutrient cycling and ultimate phosphorus removal, namely microbial communities. Accordingly, this thesis focused on understanding the microbial ecology of a pilot-scale microbial community performing EBPR to better link bioreactor processes to underlying microbial agents. Initially, temporal changes in microbial community structure and activity were monitored in a pilot-scale EBPR treatment plant by examining the ratio of small subunit ribosomal RNA (SSU rRNA) to SSU rRNA gene over a 120-day study period. Although the majority of operational taxonomic units (OTUs) in the EBPR ecosystem were rare, many maintained high potential activities, suggesting that rare OTUs made significant contributions to protein synthesis potential. Few significant differences in OTU abundance and activity were observed between bioreactor redox zones, although differences in temporal activity were observed among phylogenetically cohesive OTUs. Moreover, observed temporal activity patterns could not be explained by measured process parameters, suggesting that alternate ecological forces shaped community interactions in the bioreactor milieu. Subsequently, a metagenome was generated from pilot plant biomass samples using 454 pyrosequencing. Comparison of microbial community metabolism across multiple metagenomes from different environments revealed that EBPR community function was enriched in biofilm formation, phosphorus metabolism, and aromatic compound degradation, reflective of local bioreactor conditions. Population genomes binned from metagenomic contigs showed that M. parvicella genomes displayed remarkable genomic cohesion across EBPR ecosystems, where functional differences related to biofilm formation and antibiotic resistance, likely reflecting adaptation to habitat-specific selection pressures. Additionally, novel metabolic insights into ii Gordonia spp. in the EBPR ecosystem suggested a potential role for its involvement in polyphosphate and triacylglycerol cycling. Overall, these findings offer valuable insight on EBPR microbial ecology and will guide future studies aimed at monitoring spatiotemporal patterns in population dyanmics and gene expression. Moreover, this work demonstrates that molecular sequencing approaches can be successfully used to gain deeper insight on microbial communities responsible for wastewater remediation. iii Preface I was responsible for the design and initiation of this research program with direct input from my supervisors, Dr. Steven Hallam and Dr. Eric Hall. My thesis committee members, Dr. William Ramey, Dr. Barry Rabinowitz, and Dr. Don Mavinic, also made significant contributions to the design of the research program. In Chapter 2, I generated and analyzed the small subunit ribosomal RNA (SSU rRNA) gene amplicons and transcripts from biomass samples collected from the UBC enhanced biological phosphorus removal (EBPR) Pilot Plant. Melanie Scofield and Aria Hahn provided initial training on laboratory protocols and assisted with sample collection. Niels Hanson assisted with data visualization and provided bioinformatic support. Blake Strachan received training from me and assisted with sample collection and subsequent laboratory processing. Sam Bailey, Mike Harvard, Rony Das, and Fred Koch assisted with the operation and maintenance of the UBC EBPR Pilot Plant. I drafted the manuscript with direct input from Dr. William Ramey and Dr. Steven Hallam. Dr. Eric Hall, Dr. Barry Rabinowitz, and Dr. Don Mavinic also provided constructive feedback. Excerpts from Chapter 1 were presented at the 86th Annual Water Environment Federation Technical Exhibition and Conference, Chicago, Illinois, October 9th, 2013 and have been submitted for publication in a peer-reviewed journal: Lawson, C.E., Strachan, B.J., Hanson, N.W., Hahn, A.S., Hall, E.R., Rabinowitz, B., Mavinic, D.S., Ramey, W.D., & Hallam, S.J. Microbial community structure and activity in a pilot-scale enhanced biological phosphorus removal ecosystem. In review. In Chapter 3, I generated and analyzed the EBPR metagenome from a biomass sample collected from the UBC EBPR Pilot Plant. Masaru Nobu from the University of Illinois at Urbana-Champaign performed the metagenomic binning with my interpretation. Excerpts from iv Chapter 2 were presented at the 15th International Symposium on Microbial Ecology, Seoul, Korea, August 29th, 2014 and are in preparation for submission to a peer-reviewed journal. v Table of Contents Abstract .....................................................................................................................................ii Preface ...................................................................................................................................... iv Table of Contents ..................................................................................................................... vi List of Tables ............................................................................................................................ ix List of Figures ............................................................................................................................ x List of Symbols and Abbreviations .......................................................................................... xi Acknowledgements .................................................................................................................xiii Dedication ............................................................................................................................... xiv Chapter 1: Introduction - the microbial ecology of enhanced biological phosphorus removal ...................................................................................................................................... 1 1.1 Phosphorus: a broken biogeochemical cycle ............................................................... 1 1.2 The removal of Phosphorus from municipal wastewaters ........................................... 1 1.3 EBPR biochemical transformations and metabolic models ......................................... 2 1.4 EBPR process configurations ..................................................................................... 6 1.5 Metagenomic insights: an ecosystem model for EBPR ............................................... 7 1.5.1 Polyphosphate-accumulating organisms............................................................... 8 1.5.2 Glycogen-accumulating organisms .................................................................... 10 1.5.3 Filamentous hydrolyzing bacteria ...................................................................... 11 1.5.4 Fermenting bacteria ........................................................................................... 13 1.5.5 Denitrifying bacteria .......................................................................................... 14 1.5.6 Nitrifying bacteria ............................................................................................. 15 1.5.7 Predators: bacteriophage and protozoa ............................................................... 16 1.5.8 EBPR environments: from macro to micro......................................................... 18 1.6 Research motivation and objectives ......................................................................... 20 Chapter 2: Microbial community structure and activity in a pilot-scale EBPR ecosystem .. 22 2.1 Synopsis...................................................................................................................... 22 2.2 Background ................................................................................................................. 23 2.3 Experimental procedures ............................................................................................. 25 2.3.1 Pilot plant operation and sampling ........................................................................ 25 2.3.2 Nucleic acid extraction and cDNA synthesis......................................................... 27 vi 2.3.3 PCR amplification and pyrosequencing of SSU rDNA and cDNA ........................ 27 2.3.4 Processing of pyrotag sequences........................................................................... 28 2.3.5 Statistical analysis ................................................................................................ 28 2.4 Results ........................................................................................................................ 29 2.4.1 SSU rDNA and rRNA sequencing ........................................................................ 29 2.4.2 Overview of microbial community structure and activity .....................................
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