Date of Award

1-1-2023

Language

English

Document Type

Dissertation

Degree Name

Doctor of Philosophy (PhD)

College/School/Department

Department of Environmental Health Sciences

Content Description

1 online resource (vi, 133 pages) : illustrations (some color)

Dissertation/Thesis Chair

Samuel S Bowser

Committee Members

Katherine Alben, Xianliang Zhou, Susan Goldstein, Miriam Katz

Keywords

Heavy metals, Foraminifera, Protista

Subject Categories

Environmental Health

Abstract

Heavy metal exposure from anthropogenic pollutants negatively affects many marine organisms, including foraminiferan protists. Foraminifera are often used as bioindicators in benthic environments due to their sensitivity to environmental stress. Primary research has commonly focused on how heavy metals affect foraminiferal assemblages, distribution, ultrastructure, and shell morphology. Multi-chambered calcareous and agglutinated forams are the primary focus of such ecotoxicological studies; however, less is known about how heavy metals affect the physiology and shell microarchitecture of monothalamid agglutinated species. The research reported here represents an interdisciplinary environmental toxicology approach to study the exposure effects of heavy metal toxicants, lead (Pb) and cadmium (Cd), on oxygen respiration and shell morphogenesis in Astrammina rara, an agglutinated Antarctic monothalamid foraminifer. A. rara is an ideal model system to study these effects because it (1) is readily collected in Explorers Cove, Antarctica, a major hub of marine research in McMurdo Sound; (2) is comparable to other abundant monothalamid clades inhabiting polar and deep-sea settings; (3) is well-suited for biochemical and morphological studies due to its large size (>1 mm diameter) and ease of isolating protoplasmic and shell matrix fractions; and (4) can reconstruct its shell in vitro using artificial sediment (glass or plastic beads). The goal of this dissertation was to address several knowledge gaps regarding the use of monothalamid foraminifera as bioindicator species, and aimed to (1) determine if exposure to Pb and Cd during shell formation impacted the oxygen respiration rate of A. rara; (2) document and characterize changes in the morphology and composition of the shell after Pb and Cd exposure; and (3) identify putative metal-binding amino acids used to synthesize the agglutinated shell bioadhesive matrix. In this study, individual A. rara were dissected to remove the cell body from its native shell. For the respirometry experiments, isolated cell bodies were placed in sealed respirometry chambers with artificial sediment and normal, Pb- or Cd-spiked artificial seawater. Noninvasive oxygen-sensing optode technology was used to measure oxygen consumption during the first 24–36 h of shell formation. Compared to the baseline respiration rate in control cells, both Pb and Cd significantly suppressed the respiration rate of A. rara in all but the highest level of Pb exposure. The cells used in the shell morphogenesis exposure experiments were similarly prepared. Isolated cell bodies incubated with artificial sediment and control, Pb-, or Cd-spiked artificial seawater constructed new agglutinated shells in four weeks. SEM imaging of reconstructed shells revealed dramatic deformations in the bioadhesive of Pb-exposed shells, and less so in Cd-exposed shells. ICP-MS analysis of the isolated shells showed elevated levels of Pb, but not Cd, in the bioadhesive of treated specimens, indicating that the two metals exert their effects differentially. Finally, the bioadhesive material was collected from in vitro formed shells and hydrolyzed for amino acid analysis using ultra performance liquid chromatography (UPLC). The amino acid profile showed the presence of both sulfur-containing amino acids as well as several post-translationally modified amino acids indicative of metal-binding catechol moieties, which likely play a significant role in shell morphogenesis. Combined, these findings support including certain species of agglutinated monothalamids in marine heavy metal pollution studies, and contributes another avenue to study the global effects of Pb and Cd marine pollution in the benthic environment. Advancing the knowledge of Pb and Cd fate and transport in the marine environment is crucial for developing strategies to mitigate the effects of these global toxicants.

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