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Spatio-Temporal Distribution of Microbial Communities in the Laurentian Great Lakes

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Spatio-Temporal Distribution of Microbial Communities in the Laurentian Great Lakes SPATIO-TEMPORAL DISTRIBUTION OF MICROBIAL COMMUNITIES IN THE LAURENTIAN GREAT LAKES Mark Jeremy Rozmarynowycz A Dissertation Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY December 2014 Committee: R. Michael L. McKay, Advisor William H. O'Brien Graduate Faculty Representative George S. Bullerjahn Scott O. Rogers Zhaohui Xu ii ABSTRACT R. Michael L. McKay, Advisor Freshwater microbial communities have received comparatively little attention compared to their marine counterparts, despite the importance of these systems. Using next-generation sequencing (Illumina itags), this study examined the microbial communities of the Laurentian Great Lakes during both the summer-stratified period and during the winter. Additionally, the winter communities of the Laurentian Great Lakes were compared with the winter community of Lake Onega, one of the largest freshwater lakes in Europe. Winter communities were examined from 2010 through 2013. Lake Erie was examined during periods of high- (2010 and 2011) and low ice cover (2012). Lower ice-cover resulted in an 89% decrease in phytoplankton biovolume between years of expansive ice cover and nearly ice-free 2012. Principal coordinate analysis (PCoA) of UniFrac distance matrices revealed a strong separation between high-ice year 2010 and low-ice 2012, indicating a shift in microbial community structure. An examination of winter communities in 2013 from both Lake Erie and the upper Great Lakes revealed phylogenetically different communities for Lake Erie, Lake Michigan, and the waters of the St Mary’s River. Samples from Lake Michigan and the Straits of Mackinac clustered with Lake Erie samples, which were correlated with concentrations of chloride and sulfate. The communities of the Laurentian Great Lakes were then compared with the communities of Lake Onega, and revealed strong differences in community structure. Summer communities were examined from 2011 and 2012. A cruise from oligotrophic Lake Superior to eutrophic Lake Erie revealed differences in community structure of the surface mixed layer. Concentrations of phosphorus and ammonium were correlated with the PCoA iii plots. A comparison of the surface waters of the upper Great Lakes with their oxygenated hypolimnions revealed a unique community in deep waters. This community had high abundances of Planctomycete and Chloroflexi reads, which were stable across spatially and temporally. Resampling in 2012 confirmed the stability of this community, and also examined cyanobacterial communities in both Lake Superior and Lake Erie. The community of Lake Erie’s hypoxic ‘dead zone’ was also examined. iv Dedicated to my wife, Clair v ACKNOWLEDGMENTS I would like to thank my advisor, Dr. R. Michael L. McKay, and the members of my committee, Dr. George S. Bullerjahn, Dr. Scott O. Rogers, Dr. Zhaohui Xu, and Dr. William H. O'Brien. I would also like to thank Ben Beall, Ben Oyserman, Tim Davis, Caren Binding, Rick Bourbonniere, Michelle Palmer, Nigel D’Souza, Steve Wilhelm, Matt Saxton, Euan Reavie, Bob Sterner, Chip Small, Jacques Finlay, Sandy Brevold, Sue Watson, Michael Twiss, and Derek Smith, as well as the Technical Operations personnel from Environment Canada. A special thanks to Nikolay Filatov, Sergey Komulaynen, Yuliya Slastina, Andrei Sharov, and everyone else at the Karelian Research Center of the Russian Academy of Sciences. I would also like to thank the officers and crews of CCGS Limnos, CCGS Griffon, USCGC Neah Bay, USCGC Mackinaw, R/V Blue Heron, and R/V Lake Guardian. This material is based upon work supported by the National Science Foundation under grant no. OCE- 0927512, 0927277, and 1230735 (RMLM, GSB). Additional support was provided by the Ohio Sea Grant College Program (grant R/ER-081 to RMLM and GSB), New York Sea Grant (grant R-CE-29 to MRT), the Lake Erie Protection Fund (grant 430-12 to RMLM) and the U.S. Environmental Protection Agency (grant GL-00E00790-2 to EDR). The work conducted by the U.S. Department of Energy Joint Genome Institute was supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231 and Community Sequencing Project 723 (RMLM, GSB, RAB). vi TABLE OF CONTENTS Page INTRODUCTION: HETEROTROPHIC BACTERIA OF FRESHWATER LAKES ......... 1 CHAPTER 1: ICE COVER EXTENT DRIVES MICROBIAL COMMUNITY STRUCTURE IN A LARGE NORTH-TEMPERATE LAKE: IMPLICATIONS FOR A WARMING CLIMATE ........................................................................................................ 8 1. INTRODUCTION ................................................................................................. 8 1.1 MATERIALS AND METHODS ........................................................................ 9 1.1.1 STUDY SITE AND SAMPLING ........................................................ 9 1.1.2 HIGH-THROUGHPUT MICROBIAL COMMUNITY ANALYSIS . 11 1.2 RESULTS AND DISCUSSION .......................................................................... 14 1.2.1 LAKE PHYSICO-CHEMICAL PROPERTIES ................................... 14 1.2.2 PHYTOPLANKTON- AND MICROBIAL COMMUNITY SHIFTS ASSOCIATED WITH ICE COVER ............................................................. 15 1.2.3 ECOLOGICAL IMPLICATIONS OF LOW ICE COVER ................. 33 CHAPTER 2: TRANSITIONS IN MICROBIAL COMMUNITIES ALONG A 1,600 KM FRESHWATER TROPHIC GRADIENT ............................................................................. 35 2. INTRODUCTION ................................................................................................. 35 2.1 MATERIALS AND METHODS ........................................................................ 37 2.1.1 STUDY SITE AND SAMPLING ........................................................ 37 2.1.2 HIGH-THROUGHPUT MICROBIAL COMMUNITY ANALYSIS . 39 2.1.3 STATISTICAL ANALYSIS ................................................................ 40 2.2 RESULTS AND DISCUSSION .......................................................................... 41 2.2.1 PHYSICO-CHEMICAL PROFILES OF SAMPLING LOCATIONS 41 2.2.2 MICROBIAL COMMUNITIES ........................................................... 45 vii 2.2.3 PHYTOPLANKTON- AND MICROBIAL COMMUNITY SHIFTS ASSOCIATED WITH LAKE TROPHIC STATE ........................................ 51 2.2.4 COMMUNITIES OF THE OXYGENATED HYPOLIMNION OF THE UPPER GREAT LAKES ............................................................................... 57 2.2.5 RESAMPLING EFFORTS IN 2012 .................................................... 62 CHAPTER 3: SPATIO-TEMPORAL DYNAMICS OF WINTER MICROBIAL COMMUNITIES IN LARGE FRESHWATER LAKES ...................................................... 67 3. INTRODUCTION ................................................................................................. 67 3.1 METHODS AND MATERIALS ........................................................................ 68 3.1.1 STUDY SITES AND SAMPLING ...................................................... 68 3.1.2 HIGH-THROUGHPUT MICROBIAL COMMUNITY ANALYSIS . 70 3.1.3 STATISTICAL ANALYSIS ................................................................ 72 3.2 RESULTS AND DISCUSSION .......................................................................... 73 3.2.1 ICE CONDITIONS AND SAMPLING ............................................... 73 3.2.2 ILLUMINA SEQUENCING RESULTS .............................................. 73 3.2.3 WINTER MICROBIAL COMMUNITIES OF LAKE ERIE .............. 78 3.2.4 MICROBIAL COMMUNITIES OF THE UPPER GREAT LAKES .. 80 3.2.5 UPPER GREAT LAKES VERSES LAKE ERIE ................................ 83 3.2.6 LAKE ERIE CACHE SITES AND ICE SAMPLES ........................... 90 3.2.7 MICROBIAL COMMUNITIES OF LAKE ONEGA .......................... 91 CONCLUSIONS: ANTHROPOGENIC INFLUENCES ON FRESHWATER MICROBIAL COMMUNITIES ............................................................................................ 96 REFERENCES .......... ........................................................................................................... 98 viii APPENDIX A: TOP BLAST HITS FOR OTUS ABOVE 0.5% ABUNDANCE ................ 130 ix LIST OF FIGURES Figure Page 1 Mid-winter limnological surveys captured extremes of ice cover on Lake Erie ....... 10 2 Vertical water quality profiles for a representative central basin station (EC 1326) occupied during winter surveys of Lake Erie. ........................................................... 15 3 Phosphorus and silicate measurements ...................................................................... 16 4 Central basin phytoplankton chl a biomass ............................................................... 17 5 Phytoplankton biomass accumulation during extremes of ice cover ........................ 18 6 Rarefaction curves of observed species ..................................................................... 21 7 OTU abundance: Lake Erie 2010-12 ......................................................................... 23 8 Principal coordinate analysis: Lake Erie 2010-12 (unweighted) ............................... 25 9 Principal coordinate analysis: Lake Erie 2010-12 (weighted) ................................... 25 10 Maximum-likelihood tree of OTUs identified by supervised learning ..................... 28 11 LDA effect size cladogram: Lake Erie 2010 and 2012 ............................................. 30 12 Sampling locations: July 2011 ..................................................................................
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