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Analysis of Microbial Abundance, Metabolic Potential, and Transcriptional Activity in the Gulf of Mexico "Deadzone" Reveals an Ammonia-Oxidizing Archaeal Hotspot

Title: Analysis of Microbial Abundance, Metabolic Potential, and Transcriptional Activity in the Gulf of Mexico "Deadzone" Reveals an Ammonia-Oxidizing Archaeal Hotspot.

Inaccessible until May 31, 2021 due to copyright restrictions.

Name(s): Campbell, Lauren Gillies, author
Mason, Olivia Underwood, Professor Directing Dissertation
Miller, Thomas E., (Professor of Biological Science), University Representative
Chanton, Jeffrey P., Committee Member
Huettel, Markus, Committee Member
Knapp, Angela Noel, 1976-, Committee Member
Florida State University, degree granting institution
College of Arts and Sciences, degree granting college
Department of Earth, Ocean and Atmospheric Science, degree granting department
Type of Resource: text
Genre: Text
Doctoral Thesis
Issuance: monographic
Date Issued: 2019
Publisher: Florida State University
Place of Publication: Tallahassee, Florida
Physical Form: computer
online resource
Extent: 1 online resource (174 pages)
Language(s): English
Abstract/Description: The northern Gulf of Mexico (nGOM) is home to one of the largest eutrophication-driven seasonal hypoxic zones in the world. These hypoxic zones are also known as “dead zones” because dissolved oxygen (DO) concentrations of ≤ 2 mg L-1 are inhospitable to economically valuable fisheries. However, microorganisms flourish in “dead zones” because of their ability to utilize diverse metabolic pathways and/or by carrying out metabolic function at low oxygen concentrations. Decades worth of geochemical data has provided fine-scale resolution on nutrient and oxygen dynamics in the nGOM, however little is known about microbial community structure and activity despite the implication that microbial respiration is responsible for forming low DO conditions. To begin to fill this knowledge gap, water column samples collected across the nGOM shelf for two consecutive hypoxic seasons in July 2013 (Y13) and 2014 (Y14) were analyzed using 16S rRNA gene iTag sequencing, quantification of bacterial and thaumarchaeal 16S rRNA genes and archaeal ammonia-monooxygenase (amoA) genes using quantitative polymerase chain reaction (qPCR) assays, as well as shotgun metagenomic and metatranscriptomic sequencing of a subset of Y13 samples. In chapter two of this dissertation, analysis of the microbial community16S rRNA gene sequence data (iTag) in Y13 water column samples showed that ammonia-oxidizing Thaumarchaeota (100% similar to Nitrosopumilus maritimus) abundances were significantly enriched in hypoxic samples and inversely correlated with DO concentrations. In agreement with the iTag data, subsequent analyses of the absolute abundance (qPCR) of Thaumarchaeota 16S rRNA and amoA gene copy numbers revealed these data to be significantly more abundant in hypoxic samples and inversely correlated with DO concentrations. These results of significantly higher Thaumarchaeota abundances and amoA gene copy numbers in hypoxic samples were confirmed with analyses of Y14 data, as shown in chapter three. For both Y13 and Y14 samples, further analysis of thaumarchaeal microdiversity using oligotyping of iTag sequence data showed single nucleotide variation among Nitrosopumilus 16S rRNA gene sequences. One oligotype was significantly more abundant in hypoxic compared to oxic samples and significantly correlated with low DO, revealing a low DO adapted Nitrosopumilus oligotype in the nGOM. To better understand the ecological significance of the high thaumarchaeal abundances in the hypoxic zone shown in chapters two and three, shotgun metagenomic and metatranscriptomic sequencing was carried out on a subset of samples from Y13. Annotation of unassembled metatranscriptomic reads revealed that functional genes involved in nitrification and ammonia assimilation were some of the most abundant transcripts in both hypoxic and oxic samples, with urease enzymes being significantly more abundant in hypoxic samples. Chapter four described the physiological and metabolic activity of two novel Thaumarchaeota metagenome assembled genomes (MAGs) (estimated 79% and 96% complete). The 16S rRNA gene sequence of one MAG had a 98% identity with Nitrosopumilus maritimus SCM1 and was 100% similar to the dominant Thaumarchaeota (OTU4369009) in the Y13 nGOM. Bioinformatic analyses of these MAGs revealed that one contained transcripts coding for urea utilization, consistent with the analysis of unassembled metatranscriptomic sequences. Both MAGs recruited more metatranscriptomic reads derived from hypoxic samples (≤ 2 mg L-1) compared to oxic samples, revealing an active Thaumarchaeota population in the hypoxic zone where archaeal ammonia oxidation may be influenced by local changes in DO concentrations. Collectively, analyses of the datasets in this dissertation that include data from iTag sequencing, qPCR assays, and meta-omics sequencing, found that seasonal hypoxic conditions influenced Thaumarchaeota abundance, activity and diversity, with the annual nGOM “dead zone” emerging as a niche for low DO-adapted, cosmopolitan ammonia-oxidizing archaeal (AOA). Overall, the findings in this dissertation provided significant new insights into the ecology and biogeochemical contributions of marine Archaea, particularly in regards to the nitrogen cycle during a eutrophication-driven hypoxic event.
Identifier: 2019_Spring_Campbell_fsu_0071E_15095 (IID)
Submitted Note: A Dissertation submitted to the Department of Earth, Ocean and Atmospheric Science in partial fulfillment of the requirements for the degree of Doctor of Philosophy.
Degree Awarded: Spring Semester 2019.
Date of Defense: April 2, 2019.
Keywords: Ammonia oxidation, Archaea, Dead zones, Gulf of Mexico, iTag, Metagenomics
Bibliography Note: Includes bibliographical references.
Advisory Committee: Olivia U. Mason, Professor Directing Dissertation; Thomas E. (Tom) Miller, University Representative; Jeffrey P. Chanton, Committee Member; Markus Huettel, Committee Member; Angela Knapp, Committee Member.
Subject(s): Marine biology
Environmental sciences
Persistent Link to This Record:
Host Institution: FSU

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Campbell, L. G. (2019). Analysis of Microbial Abundance, Metabolic Potential, and Transcriptional Activity in the Gulf of Mexico "Deadzone" Reveals an Ammonia-Oxidizing Archaeal Hotspot. Retrieved from