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Bacterioplankton in the Oregon Upwelling System: Distribution, Cell

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Bacterioplankton in the Oregon Upwelling System: Distribution, Cell AN ABSTRACT OF THE DISSERTATION OF Krista Longnecker for the degree of Doctor ofPhilosophy in Oceanography presented on July 2, 2004. Title: Bacterioplankton in the Oregon UpwellingSystem: Distribution, Cell-specific Leucine Incorporation, and Diversity Abstract approved: Redacted for privacy Barry F. Sherr Marine bacterioplankton playan important role in global elemental cycles because they return carbon dioxide and nutrientsto the biosphere as they reduce organic matter. Furthermore, marine bacterioplanktonare not unifonnly active, and subpopulations of the in situ communitymay be more or less active at any given time. Defining whether or not a cell is 'active' isnot without difficulty, and the result varies depending on the assay used, since differentassays examine different physiological processes within a cell. Linking the level of activity ofa cell with its phylogenetic identity is an additional important step inexamination of the role of marine prokaryotes in global elemental cycles. In this project,flow cytometry was used in two ways to examine relative cell-specific metabolic activity inbacterioplankton cells: as relative cell-specific nucleic acidcontent via staining with SYBR Green I, andas ability to reduce sufficient 5-cyano-2,3-ditolyltetrazolium chloride (CTC) to be identified as having an active electrontransport system. Based on flow cytometric sorting of cells labeled with 3H-leucine, thehigh nucleic acid (HNA) cells had higher cell-specific leucine incorporation rates than thelow nucleic acid (LNA) cells. The HNA cells were also responsible for proportionatelymore of the leucine incorporation by the total heterotrophic population. Whilethe CTC-positive cells had higheraverage cell-specific leucine incorporation rates than theHNA cells, their low abundances meant that they were responsible for less than 15% ofthe total leucine incorporation. The diversity ofBacteriaobserved within the HNA and LNA assemblageswas examined using phylogenetic analysis based on the V3-V4-V5 variable regions of16S rRNA genes. Most of the phylogenetic groups ofBacteriaidentified in this study were present in both the HNA and LNA assemblage and had, at times,an active electron transport system (i.e., were able to reduce CTC). Finally, non-metric multidimensional scaling was presented as a new method to analyze DNAsequence data in conjunction with measured environmental parameters. ©Copyright by Krista Longnecker July 2, 2004 All Rights Reserved Bactenoplankton in the Oregon Upwelling System: Distribution,Cell-specific Leucine Incorporation, and Diversity L Krista Longnecker A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented July 2, 2004 Commencement June 2005 Doctor of Philosophy dissertation of Krista Longnecker presented on July 2, 2004 APPROVED: Redacted for privacy Major Professor, representing Oceanography Redacted for privacy Dean of the College of Oceanic and Atmospheric Sciences Redacted for privacy Dean of G±aauate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release ofmy dissertation to any reader upon request. Redacted for privacy Krista Longnecker, Author ACKNOWLEDGMENTS I greatly appreciate the guidance I have received from Barry Sherr and Evelyn Sherr, guidance which began at the very start ofmy time at COAS. Barry has shown me that crazy ideas are possible and valid ways to address questions, while Ev's consideration of this project in light of other research in thearea is very much appreciated. My other committee members (Kate Field, Steve Giovannoni,Wayne Huber, and Ricardo Letelier) have also asked intriguing and insightfulquestions about the research and I appreciate their input into this project. Oregon State University, and in particular COAS, has beena tremendous place to be a graduate student, because of the faculty, the other students, and the behindthe scenes support of different parts of the administration. I thank Charlie Miller for making me raise questions about other people's research andmy own research. Bruce McCune of the botany department gaveme an excellent grounding in multivariate statistics through his class and by patiently answering questionseven after the end of the term. I was lucky to arrive at COAS with a great cohort of students. Perhapssome day there will be a new research institute representing therange of scientific questions that can be answered by Mark Baumgartner, Lisa Eisner, JaimeGómez-Gutiérrez, Sam Laney, Daniel Palacios, and Malinda Sutor. Certainly I have enjoyedboth the science and non-science discussions with thisgroup and their significant others, and I look forward to working with all of them in the future. Along the way towards obtainingmy degree, I received help and ship time from other people which I greatly appreciate. The ground workfor the research presented in Chapters Two and Four was initially conducted in2001 on a series of day-long cruises on theRV Elakha. Iwould like to thank Tim Cowles' lab for the opportunity to participate on those cruises. Two undergraduates,Maike Lichtenberg and Delfina Homen, were extremely helpful, and I would stillworking in the lab if not for their help. Finally, all of the data presented herewere generated from samples collected during a 2002 cruise on the RVWecoma. Ithank the captain, crew, and marine technicians of the RVWecomafor their assistance during the cruise and the other cruise participants. The opportunity to participateon a cruise with a group of researchers interested in answering thesame question, but using different methods, was wonderful. I also enjoyed the discussions during and following the cruise, and think that the broader implications of this project became muchclearer thanks to their input. This research was funded byNSF OCE-0002236andOCE-0240785toB.F.S. andE.B.S.,and additional support for laboratory equipmentcame from an OSU Research Equipment Reserves Fund grant. CONTRIBUTION OF AUTHORS Drs. Barry Sherr and Evelyn Sherr contributed to the collection of the data, its analysis, and the editing of Chapters Two and Four of this dissertation. TABLE OF CONTENTS Page 1 Introduction...............................................................................................................1 1.1 Background...........................................................................................1 1.1.1Methods used to identify cells as 'active'.................................2 1.1.2Using 1 6S rRNA genes to identify marine prokaryotes...........8 1.1.3Analysis of DNA sequence data in an ecological context........9 1.2 Research objectives and summary of results......................................10 1.3 Literature cited.................................................................................... 12 2 High nucleic acid, low nucleic acid, and CTC-positive bacterial cells in an upwelling ecosystem: distribution and cell-specific leucine incorporation. ...22 2.1 Abstract............................................................................................... 22 2.2 Introduction......................................................................................... 22 2.3 Materials and Methods........................................................................ 26 2.3.1Sample collection and oceanographic parameters..................26 2.3.2Environmental parameters...................................................... 27 2.3.3Determining cell abundance using the flow cytometer...........28 2.3.4Abundance of cells with an active electron transport system ...................................................................................... 30 2.3.5Whole seawater volumetric leucine incorporation..................30 2.3.6Flow cytometric sorting of cells labeled with 3H-leucine.......31 2.3.7Nonmetric multidimensional scaling......................................34 2.3.8Statistical analysis................................................................... 34 2.4 Results................................................................................................. 37 2.4.1Regional hydrography during sampling..................................37 2.4.2Cell abundance dataheterotrophic and photoautotrophic cells............................................................. 39 TABLE OF CONTENTS (CONTINUED) 2.4.3Whole seawater volumetric leucine incorporation..................42 2.4.4Cell-specific leucine incorporation rates.................................43 2.4.5Cell-specific leucine incorporation by CTC-positive cells.........................................................................................47 2.4.6Sorted volumetric leucine incorporation rates........................49 2.4.7Comparisons to environmental parameters.............................54 2.4.8Spatial variability in distribution of cell-specific activity.......54 2.5 Discussion........................................................................................... 54 2.5.1Leucine incorporation rates in whole seawater compared to rates in ITNA or LNA cells................................................. 55 2.5.2CTC as a proxy to identify metabolically active bacterioplankton...................................................................... 57 2.5.3Relationship between variability in rates of leucine incorporation and environmental parameters.......................... 58 2.5.4Distribution of flow cytometrically-defined microorganisms......................................................................
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