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INTERACTIONS of CYANOBACTERIA and CO-OCCURRING MICROORGANISMS DURING CYANOBACTERIAL HARMFUL ALGAL BLOOMS a Dissertation Submitte

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INTERACTIONS of CYANOBACTERIA and CO-OCCURRING MICROORGANISMS DURING CYANOBACTERIAL HARMFUL ALGAL BLOOMS a Dissertation Submitte INTERACTIONS OF CYANOBACTERIA AND CO-OCCURRING MICROORGANISMS DURING CYANOBACTERIAL HARMFUL ALGAL BLOOMS A dissertation submitted to Kent State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Kai Wang May 2021 © Copyright All rights reserved Except for previously published materials Dissertation written by Kai Wang B.S., Sichuan Agricultural University, 2012 M.S., Ocean University of China, 2015 Ph.D., Kent State University, 2021 Approved by Xiaozhen Mou, Ph.D. , Chair, Doctoral Dissertation Committee Helen Piontkivska, Ph.D. , Members, Doctoral Dissertation Committee David Costello, Ph.D. Hanbin Mao, Ph.D. Joseph Ortiz, Ph.D. Accepted by Laura G. Leff, Ph.D. , Chair, Department of Biological Sciences Mandy Munro-Stasiuk, Ph.D., Interim Dean, College of Arts and Sciences TABLE OF CONTENTS TABLE OF CONTENTS ......................................................................................................... iii LIST OF FIGURES ................................................................................................................... v LIST OF TABLES .................................................................................................................... ix ACKNOWLEDGEMENTS ....................................................................................................... x I. GENERAL INTRODUCTION ................................................................................ 1 REFERENCES ............................................................................................ 14 II. CYANOBACTERIAL BLOOMS ALTER THE RELATIVE IMPORTANCE OF NEUTRAL AND SELECTIVE PROCESSES IN ASSEMBLING FRESHWATER BACTERIOPLANKTON COMMUNITY ............................................................ 25 PREFACE ................................................................................................... 25 ABSTRACT ................................................................................................ 25 INTRODUCTION ...................................................................................... 26 MATERIALS AND METHODS ................................................................ 29 RESULTS .................................................................................................... 36 DISCUSSION ............................................................................................. 44 CONCLUSIONS ......................................................................................... 49 REFERENCES ............................................................................................ 51 III. CO-OCCURRING MICROORGANISMS REGULATE THE SUCCESSION OF CYANOBACTERIAL HARMFUL ALGAL BLOOMS ....................................... 83 PREFACE ................................................................................................... 83 iii ABSTRACT ................................................................................................ 83 INTRODUCTION ...................................................................................... 84 MATERIALS AND METHODS ................................................................ 87 RESULTS .................................................................................................... 93 DISCUSSION ........................................................................................... 102 CONCLUSIONS ....................................................................................... 106 REFERENCES .......................................................................................... 108 IV. COORDINATED DIEL GENE EXPRESSION OF CYANOBACTERIA AND THEIR MICROBIOME ....................................................................................... 140 PREFACE ................................................................................................. 140 ABSTRACT .............................................................................................. 140 INTRODUCTION .................................................................................... 141 MATERIALS AND METHODS .............................................................. 143 RESULTS .................................................................................................. 149 DISCUSSION ........................................................................................... 156 CONCLUSIONS ....................................................................................... 160 REFERENCES .......................................................................................... 161 V. SUMMARY ......................................................................................................... 177 REFERENCES .......................................................................................... 183 iv LIST OF FIGURES Figure 1 Average abundances of estimated microbial communities. ....................................... 60 Figure 2 Time-lag regression analysis of microbial communities. .......................................... 61 Figure 3 Fit of the neutral model. ............................................................................................ 62 Figure 4 (a) The estimated migration rate, (b) Neutral and non-neutral partitions of the bacterioplankton communities, (c) List of non-neutral bacterioplankton genera. ................... 63 Figure 5 Relationship between the measured environmental parameters and bacterioplankton communities based on (a) all samples and (b) only non-bloom samples, (c) Heatmap of Pearson’s correlation coeFficient values. .................................................................................. 64 Figure 6 (a) The co-occurrence patterns among bacterioplankton communities, cyanobacterial, planktonic algae, and zooplankton cell abundances, (b-g) Ternary plots showing relative abundance from modules 1-6 in the three diFferent periods. ........................ 65 Figure 7 Rarefaction curves of operational taxonomic unit at 97% sequence similarity level. .................................................................................................................................................. 66 Figure 8 Temporal distribution pattern of bacterioplankton alpha diversity indexes. ............. 67 Figure 9 Time-lag regression analysis of bacterioplankton communities at (a) phylum, (b) class, (c) order, (d) family, and (e) genus levels. ..................................................................... 68 Figure 10 The relative contribution of measured environmental parameters on (a) cyanobacterial, (b) planktonic algae, and (c) zooplankton communities. ................................ 69 Figure 11 Distance-based linear redundancy visualizing the relative contribution of measured environmental parameters on (a) non-neutral OTUs, and (b) neutral OTUs. .......................... 70 v Figure 12 The distributions of degree for the microbial community co-occurrence network (green) and Erdös-Rényi random network (orange). ............................................................... 71 Figure 13 Zi-Pi plot showing the distribution of bacterioplankton OTUs based on their topological roles. ...................................................................................................................... 72 Figure 14 Network visualizing significant correlations between measured biotic and abiotic variables. .................................................................................................................................. 73 Figure 15 Temporal dynamics of (a) cyanobacterial genera and (b) their associated microbiome organisms, (c) Correlation analysis of cyanobacterial abundances, (d) PCA analysis of cyanobacterial metatranscriptomes. ..................................................................... 116 Figure 16 Environmental variables during sampling period in Harsha Lake. ....................... 117 Figure 17 DiFferentially expressed cyanobacterial genes in metabolisms of (a) Nitrogen, (b) Phosphorus, (c) Gas vesicle, (d) Extracellular polysaccharide, and (e) Secondary metabolites. ................................................................................................................................................ 118 Figure 18 WGCNA networks of (a) Anabaena, (b) Microcystis, (c) Planktothrix, (d) non- cyanobacterial, and (e) cyanophage gene expression matrices. ............................................. 119 Figure 19 (a) The WGCNA approach directly links (a) Ana1 and (c) NC8 module structures to Anabaena biomass; sPLS regression was used to predict Anabaena biomass. .................. 120 Figure 20 Temporal change of averaged expression levels of genes of the enriched GO terms within the (a) Ana1, and (c) NC8 modules. The value importance in projection values. ...... 121 Figure 21 (a) The WGCNA approach directly links (a) Mic4, (c) Mic6, (e) Mic7, (g) NC2, and (i) CP9 module structures to Microcystis biomass; sPLS regression was used to predict vi Microcystis biomass. .............................................................................................................. 122 Figure 22 Temporal change of averaged expression levels of genes of the enriched GO terms within the (a) Mic4, Mic6, Mic7, (c) NC2 modules, and (e) CP9 module. The value importance in projection values. ............................................................................................ 123 Figure 23 The WGCNA approach directly links (a) Pla12, (c) NC5, and (e) CP8 module structures to Planktothrix
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