Biogeochemical mercury cycling in sea ice and geothermal springs

© 2016 Dr. Caitlin Marissa Gionfriddo Microorganisms strongly influence the environmental form and fate of mercury. Recent advancements in culture-independent molecular techniques, such as high-throughput sequencing, allow us to delve deeply into the functional and phylogenetic composition of enviro...

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Main Author: Gionfriddo, Caitlin Marissa
Format: Doctoral or Postdoctoral Thesis
Language:unknown
Published: 2016
Subjects:
Online Access:http://hdl.handle.net/11343/150616
id ftumelbourne:oai:jupiter.its.unimelb.edu.au:11343/150616
record_format openpolar
institution Open Polar
collection The University of Melbourne: Digital Repository
op_collection_id ftumelbourne
language unknown
topic mercury
methylmercury
microbial mercury resistance
biogeochemistry
Antarctic
sea ice
geothermal
metagenomics
microbial diversity
spellingShingle mercury
methylmercury
microbial mercury resistance
biogeochemistry
Antarctic
sea ice
geothermal
metagenomics
microbial diversity
Gionfriddo, Caitlin Marissa
Biogeochemical mercury cycling in sea ice and geothermal springs
topic_facet mercury
methylmercury
microbial mercury resistance
biogeochemistry
Antarctic
sea ice
geothermal
metagenomics
microbial diversity
description © 2016 Dr. Caitlin Marissa Gionfriddo Microorganisms strongly influence the environmental form and fate of mercury. Recent advancements in culture-independent molecular techniques, such as high-throughput sequencing, allow us to delve deeply into the functional and phylogenetic composition of environmental microbial communities. Metagenomic techniques can be used to link the distribution of microbes equipped with mercury cycling genes to environmental processes, such as the production of the toxin, methylmercury. Presented in this thesis are metagenomic-sequencing data (Illumina Hiseq 2 x 100-bp paired-end technology) from two mercury-enriched environments: Antarctic sea ice and brine, and acidic geothermal springs. Metagenomic analyses are paired with geochemical analyses to examine how various physicochemical parameters may impact microbial community structure and function as it relates to mercury cycling. Both environments exhibit microbial communities equipped with various adaptive mechanisms, including the mercury detoxifying mer-operon amongst other metal and stress resistance pathways. Furthermore, close analogues of mercury methylation genes (hgcAB) are detected alongside the mer detoxification pathway in both environments, indicating an active methylation-demethylation-reduction cycling of mercury by these microbial communities. In polar marine environments, the long-range atmospheric transport of inorganic mercury, and an active atmospheric cycling of mercury following polar sunrise, results in the deposition of mercury onto sea-ice covered waters of the Southern Ocean. Sea-ice covered waters and the fauna that inhabit them tend to have inflated concentrations of the bioaccumulative neurotoxin, methylmercury, compared to open ocean waters. However, the role of sea ice in biogeochemical mercury cycling is poorly understood, particularly the production of methylmercury. In this thesis, deep metagenomic sequencing is used to identify potential microbial transformations of mercury in first-year sea ice and brine sampled from East Antarctica. Measured concentrations of total and methylated mercury in the sea-ice environment ranged from 1.01 to 895 pM, and <0.1 to 0.80 pM, respectively. Heterotrophic bacteria and photoautotrophic eukaryotes dominated the metagenomic datasets; however, chemoautotrophic archaea and bacteria were also present at lower abundance within the sea-ice and brine communities. Mercuric reductase genes (merA) closely related to those of Proteobacteria were identified in brine and ice communities. Metagenomic screening for mercury methylation genes (hgcAB) showed similarity (>50%) to highly conserved sites of hgcA. The putative methylation gene belongs to Nitrospina, and is predicted to encode an HgcA-like pterin-binding enzyme in the family of cobalamin-dependent methyltransferase. This study shows that the toxin, methylmercury, may be microbially produced within sea ice, constituting a source of the toxin to the Southern Ocean ecosystem. This work suggests, for the first time, that microbial mercury methylation can occur in a low oxygen environment, and implicates a common marine nitrite-oxidizer in the production of methylmercury. This thesis presents new information on how the structure and functionality of sea-ice microbial communities impact mercury transformations in polar environments. Few studies have explored the microbial underpinnings of mercury transformations in geothermal settings. Yet, hot springs and fumaroles release significant quantities of aqueous and gaseous mercury into the environment. Presented here are results from metagenomic sequencing of geothermal microbial communities cycling mercury, focusing on the connections between putative metabolisms and mercury methylation, and mercury demethylation and reduction in contaminated sediments. Presented are data from two adjacent, acidic (pH<3), mesothermal (22-40.5 °C) hot springs of the Ngawha Geothermal Field (Northland, New Zealand), extremely enriched in total mercury (>1000 ng L-1), and varying MeHg concentrations (1-10 ng L-1). Acidophilic, thermophilic, sulfur-cycling, and iron-cycling bacteria and archaea dominate microbial communities of both springs. Although genes of the mer operon were detected in both springs (at high abundance), mercury methylation genes (hgcAB) were only detected in the cooler spring (ΔT~10°C), with an order of magnitude greater methylmercury. The hgcAB genes have no known closest relative, but most likely belong to an uncultured acidophilic, sulfate-reducing bacterium. This study shows that geothermal microbial communities are capable of net production of methylmercury, alongside active demethylation-reduction by mer-capable microbes, despite selective pressures from low pH and high mercury levels. However, temperature may be a major limiting factor on the presence and activity of mercury methylating microorganisms in the environment.
format Doctoral or Postdoctoral Thesis
author Gionfriddo, Caitlin Marissa
author_facet Gionfriddo, Caitlin Marissa
author_sort Gionfriddo, Caitlin Marissa
title Biogeochemical mercury cycling in sea ice and geothermal springs
title_short Biogeochemical mercury cycling in sea ice and geothermal springs
title_full Biogeochemical mercury cycling in sea ice and geothermal springs
title_fullStr Biogeochemical mercury cycling in sea ice and geothermal springs
title_full_unstemmed Biogeochemical mercury cycling in sea ice and geothermal springs
title_sort biogeochemical mercury cycling in sea ice and geothermal springs
publishDate 2016
url http://hdl.handle.net/11343/150616
geographic Antarctic
East Antarctica
New Zealand
Southern Ocean
geographic_facet Antarctic
East Antarctica
New Zealand
Southern Ocean
genre Antarc*
Antarctic
Antarctica
East Antarctica
Sea ice
Southern Ocean
ice covered waters
genre_facet Antarc*
Antarctic
Antarctica
East Antarctica
Sea ice
Southern Ocean
ice covered waters
op_relation http://hdl.handle.net/11343/150616
op_rights Terms and Conditions: Copyright in works deposited in Minerva Access is retained by the copyright owner. The work may not be altered without permission from the copyright owner. Readers may only download, print and save electronic copies of whole works for their own personal non-commercial use. Any use that exceeds these limits requires permission from the copyright owner. Attribution is essential when quoting or paraphrasing from these works.
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spelling ftumelbourne:oai:jupiter.its.unimelb.edu.au:11343/150616 2023-05-15T14:03:39+02:00 Biogeochemical mercury cycling in sea ice and geothermal springs Gionfriddo, Caitlin Marissa 2016 http://hdl.handle.net/11343/150616 unknown http://hdl.handle.net/11343/150616 Terms and Conditions: Copyright in works deposited in Minerva Access is retained by the copyright owner. The work may not be altered without permission from the copyright owner. Readers may only download, print and save electronic copies of whole works for their own personal non-commercial use. Any use that exceeds these limits requires permission from the copyright owner. Attribution is essential when quoting or paraphrasing from these works. mercury methylmercury microbial mercury resistance biogeochemistry Antarctic sea ice geothermal metagenomics microbial diversity PhD thesis 2016 ftumelbourne 2019-10-15T12:20:07Z © 2016 Dr. Caitlin Marissa Gionfriddo Microorganisms strongly influence the environmental form and fate of mercury. Recent advancements in culture-independent molecular techniques, such as high-throughput sequencing, allow us to delve deeply into the functional and phylogenetic composition of environmental microbial communities. Metagenomic techniques can be used to link the distribution of microbes equipped with mercury cycling genes to environmental processes, such as the production of the toxin, methylmercury. Presented in this thesis are metagenomic-sequencing data (Illumina Hiseq 2 x 100-bp paired-end technology) from two mercury-enriched environments: Antarctic sea ice and brine, and acidic geothermal springs. Metagenomic analyses are paired with geochemical analyses to examine how various physicochemical parameters may impact microbial community structure and function as it relates to mercury cycling. Both environments exhibit microbial communities equipped with various adaptive mechanisms, including the mercury detoxifying mer-operon amongst other metal and stress resistance pathways. Furthermore, close analogues of mercury methylation genes (hgcAB) are detected alongside the mer detoxification pathway in both environments, indicating an active methylation-demethylation-reduction cycling of mercury by these microbial communities. In polar marine environments, the long-range atmospheric transport of inorganic mercury, and an active atmospheric cycling of mercury following polar sunrise, results in the deposition of mercury onto sea-ice covered waters of the Southern Ocean. Sea-ice covered waters and the fauna that inhabit them tend to have inflated concentrations of the bioaccumulative neurotoxin, methylmercury, compared to open ocean waters. However, the role of sea ice in biogeochemical mercury cycling is poorly understood, particularly the production of methylmercury. In this thesis, deep metagenomic sequencing is used to identify potential microbial transformations of mercury in first-year sea ice and brine sampled from East Antarctica. Measured concentrations of total and methylated mercury in the sea-ice environment ranged from 1.01 to 895 pM, and <0.1 to 0.80 pM, respectively. Heterotrophic bacteria and photoautotrophic eukaryotes dominated the metagenomic datasets; however, chemoautotrophic archaea and bacteria were also present at lower abundance within the sea-ice and brine communities. Mercuric reductase genes (merA) closely related to those of Proteobacteria were identified in brine and ice communities. Metagenomic screening for mercury methylation genes (hgcAB) showed similarity (>50%) to highly conserved sites of hgcA. The putative methylation gene belongs to Nitrospina, and is predicted to encode an HgcA-like pterin-binding enzyme in the family of cobalamin-dependent methyltransferase. This study shows that the toxin, methylmercury, may be microbially produced within sea ice, constituting a source of the toxin to the Southern Ocean ecosystem. This work suggests, for the first time, that microbial mercury methylation can occur in a low oxygen environment, and implicates a common marine nitrite-oxidizer in the production of methylmercury. This thesis presents new information on how the structure and functionality of sea-ice microbial communities impact mercury transformations in polar environments. Few studies have explored the microbial underpinnings of mercury transformations in geothermal settings. Yet, hot springs and fumaroles release significant quantities of aqueous and gaseous mercury into the environment. Presented here are results from metagenomic sequencing of geothermal microbial communities cycling mercury, focusing on the connections between putative metabolisms and mercury methylation, and mercury demethylation and reduction in contaminated sediments. Presented are data from two adjacent, acidic (pH<3), mesothermal (22-40.5 °C) hot springs of the Ngawha Geothermal Field (Northland, New Zealand), extremely enriched in total mercury (>1000 ng L-1), and varying MeHg concentrations (1-10 ng L-1). Acidophilic, thermophilic, sulfur-cycling, and iron-cycling bacteria and archaea dominate microbial communities of both springs. Although genes of the mer operon were detected in both springs (at high abundance), mercury methylation genes (hgcAB) were only detected in the cooler spring (ΔT~10°C), with an order of magnitude greater methylmercury. The hgcAB genes have no known closest relative, but most likely belong to an uncultured acidophilic, sulfate-reducing bacterium. This study shows that geothermal microbial communities are capable of net production of methylmercury, alongside active demethylation-reduction by mer-capable microbes, despite selective pressures from low pH and high mercury levels. However, temperature may be a major limiting factor on the presence and activity of mercury methylating microorganisms in the environment. Doctoral or Postdoctoral Thesis Antarc* Antarctic Antarctica East Antarctica Sea ice Southern Ocean ice covered waters The University of Melbourne: Digital Repository Antarctic East Antarctica New Zealand Southern Ocean