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Indentification, Enumeration and Diversity of Nitrifying Bacteria in the Laurentian Great Lakes

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Indentification, Enumeration and Diversity of Nitrifying Bacteria in the Laurentian Great Lakes IDENTIFICATION, ENUMERATION AND DIVERSITY OF NITRIFYING BACTERIA IN THE LAURENTIAN GREAT LAKES Anirban Ray A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirement for the degree of MASTER OF SCIENCE December 2012 Committee: Dr. George Bullerjahn, Advisor Dr. Robert Michael McKay Dr. Zhaohui Xu © 2012 Anirban Ray All Rights Reserved iii ABSTRACT Dr. George Bullerjahn, Advisor In the past 100 years the nitrate levels in Lake Superior have increased more than five times (Sterner et al. 2007). Based on stable isotope assays, previous research has shown that most of this nitrate is coming from in-lake nitrification process in the lake (Finlay et al. 2007), reflecting an imbalanced nitrogen cycle. By contrast, in Lake Erie the nitrate levels are declining. Lake Erie is the shallowest of the Great Lakes. The shallowness of the lake, the warmer temperature of the water, and nutrient inputs from urban and agricultural sources make it most biologically productive of the Great lakes. Nitrification is a major process in the nitrogen cycle mainly carried out by the nitrifying microbial community (both Archaea and Bacteria), during which ammonia (NH3) - - is converted to Nitrite (NO2 ) and then to nitrate (NO3 ) by ammonia oxidizers (both Bacteria and Archaea) and Nitrite oxidizers (Bacteria only) respectively. Ammonia is oxidized by the enzyme ammonia monooxygenase, and hydroxylamine oxidoreductase - – (HAO). Nitrite (NO2 ) converted to nitrate (NO3 ) by Nitrite oxidizers (Bacteria) and enzyme nitrite oxidoreductase, carries this reaction. In this thesis, I investigated the microbial nitrifier community structure by identifying and enumerating the ammonia-oxidizing bacteria (AOB) and nitrite oxidizing bacteria (NOB) present in these two lakes using the technique of fluorescence in-situ hybridization (FISH). This is the first study on Lake Superior and Lake Erie proving the overview of the abundance and diversity of these organisms. This study is focusing on iv understanding the nitrifying microbial community structure, contribution to other studies dealing with how these organisms function in the nitrogen cycling in these lakes. Therefore, the goal of this study is to provide measure of abundance of AOB and NOB in Lake Superior and Lake Erie as well as the diversity of AOB in these lakes. v Dedicated to the memory of my mother Mrs. Nupur Ray, who could not be there to see this day of my life. vi ACKNOWLEDGMENTS First and foremost, I want to extend my deep appreciation for my thesis advisor and mentor Dr. George Bullerjahn for all his guidance and patience throughout the two years I spent in his laboratory. Without him, this thesis will not be possible. Words are not enough to express my thankfulness to him for accepting me in his lab, and for the invaluable advice and his immense tolerance and understanding of every stupid mistake I made in the lab. Thank you for being an invaluable resource to my academic life, and also for providing constant motivation to do quality work, all the time providing an immense level of independence to do my work on my own. I want to thank my co-advisor Dr. Mike Mckay for his continuous support and advice in this work throughout. I also want to extend my gratitude to my thesis committee member Dr. Zhaohui Xu for accepting to be a member of my committee, and for her inputs in this thesis. I would like to specially thank all the members of the Bullerjahn-McKay lab, Maitreyee Mukherjee, Mike Schlais, Mark Rozmarynowycz, Nigel D’Souza, Zhi Zhu, Benjamin Beall, and Olga Kutovaya. Thank you all for the helpful suggestions you gave me and for your friendship. A special thanks goes to my lovely wife for believing in me, for her immense understanding and patience, and for her valuable advices. Last but not the least; I want to thank my parents and my friends in the US and in India for supporting me all through this time. Thank you all very much for everything. vii TABLE OF CONTENTS Page INTRODUCTION .... ........................................................................................................... 1 MATERIAL AND METHODS ............................................................................................ 14 Study sites ........................................................................................................ 14 Catalyzed reporter deposition- fluorescence in-situ hybridization (CARD-FISH) ........................................................................................................... 18 Sample processing ......................................................................................... 18 Fluorescently labeled probes ......................................................................... 18 Permeabilization…………………………………………………………….. 20 Hybridization ................................................................................................ 20 Tyramide amplification ................................................................................. 23 Microscopy ........................................................................................................... 23 Polymerase chain reaction (PCR) ............................................................................. 24 PCR amplification of the amoA gene fragment ............................................ 24 PCR amplification of the 16S rRNA gene .................................................... 25 Cloning, sequencing and phylogeny inference……………………………………... 25 RESULT……………………………………………………………………………............ 27 In-situ characterization of the nitrifying bacterial population in Great lakes………. 27 NOB in Lake Superior: 2010……………………………………………………….. 29 NOB in Lake Superior: 2011……………………………………………………….. 31 AOB in Lake Superior: 2011……………………………………………………….. 33 viii NOB in Lake Erie: 2011…………………………………………………………….. 35 AOB in Lake Erie: 2011………………………………………………………….. 37 Bacterial amoA diversity study in Great lakes……………………………………… 39 DISCUSSION……………………………………………………………………………… 44 REFERENCES……………………………………………………………………………. 49 ix LIST OF FIGURES Figure Page 1 Biological Nitrogen Cycle......................................................................................... 5 2 Basic steps of fluorescence in-situ hybridization (FISH)…………………………… 11 3 General principle of the catalyzed reporter deposition-FISH (CARD-FISH)............ 13 4 Map of the study sites: Lake Superior....................................................................... 15 5 Map of the study sites: Lake Erie .............................................................................. 16 6 FISH images……………………………………………………………………….. 28 7 Total NOB cells per mL measured from Lake Superior: 2010 ................................. 32 8 Total NOB cells per mL measured from Lake Superior: 2011 ................................. 34 9 Total AOB cells per mL measured from Lake Superior: 2011 ................................. 36 10 Total NOB cells per mL measured from Lake Erie: 2011…...…………………… . 38 11 Total AOB cells per mL measured from Lake Erie: 2011………………………. ... 40 12 PCR amplification of amoA gene sequences from Lake Superior (Station CD1) and Lake Erie (Station CCB3)………………………………………………………. 41 13 Bacterial amoA colony PCR product from Lake Superior and Lake Erie…………... 42 14 Phylogenetic tree based on amoA sequences from Lake Superior…………………... 43 15 Phylogenetic tree based on amoA sequences from Lake Erie……………………….. 44 x LIST OF TABLES Table Page 1 Lake Superior and Lake Erie sampling stations LAT/LONG………………… ........ 17 2 Oligonucleotide probe sequences used for FISH in this study……………………… 19 3 Standard hybridization Buffer used for FISH in this study…………………………. 22 4 Standard Washing Buffer used for FISH in this study………………………........... 26 1 1. INTRODUCTION 1.1 Nitrification Approximately 78.09% by volume of Earth’s atmosphere is constituted of dinitrogen gas (N2), which cannot be used directly by most organisms. Over the past evolutionary history only a few bacteria and archaea have developed the ability to convert dinitrogen into ammonia (NH3). Nitrogen is one the most important elements for life, because it is a major component in proteins and nucleic acids. Nitrogen can exist in numerous oxidation states from the +5 state (nitrate) to -3 state (ammonium and amino-nitrogen), hence nitrogen can act as an electron donor as well as an electron acceptor. The nitrogen cycle gains particular interest in the many environments because nitrogen can be a limiting nutrient to primary producers. The nitrogen cycle consists of several steps that include nitrogen fixation, ammonium oxidation, assimilatory and dissimilatory nitrate reduction, ammonification, denitrification and ammonium assimilation (Fig.1). The biological process where ammonia is oxidized as an energy source to nitrate is called nitrification (Fig. 1). Although nitrification is carried out by the aerobic obligate chemolithoautotrophs, some methylotrophs and a few heterotrophic fungi and bacteria can also perform this oxidation. In anaerobic niches, ammonia produced by the deamination of amino acids, urea, or uric acids or via dissimilatory nitrate reduction diffuses into the aerobic environment, where it is oxidized by the aerobic nitrifiers. The aerobic nitrifying microbes are often found at the junction between aerobic – anaerobic interfaces, where they capture the ammonia as it diffuses from the anaerobic environments (Strous, M., and M. S. M. Jetten. 2004) 2 The nitrification process is carried out in two steps. At first
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