Lipid biomarkers of coral stress : calibration and exploration

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution June 2011Corals are increasingly threatened by warming sea surface temperatures and other anthropogenic changes. The delicate symbiosis between corals and their algal endosymbionts (zooxanthellae) is easily disrupted by thermal stress, leading to bleaching and eventual mortality. The use of lipid ratios as biomarkers of environmental conditions is well established. Coral biomass contains abundant lipids, and the potential of lipid parameters to diagnose thermal tolerance in zooxanthellae has been previously suggested. In this thesis, I explore the response of specific fatty acids, sterols, and thylakoid membrane lipids to thermal and disease stress in zooxanthellae grown in culture, as well as those isolated from living corals. I present the discovery of a bioactive thylakoid lipid within zooxanthellae cells, and show how this compound is selectively mobilized in thermally stressed cells. I present a plausible mechanism for the breakdown of this compound into products that may cause apoptosis and disrupt the coral-­‐algal symbiosis, eventually causing bleaching. I present two new lipid biomarkers of thermal stress in zooxanthellae, the C18 fatty acid unsaturation ratio, and the fatty acid to sterol ratio. I calibrate the decline of these two parameters to levels of thermal stress comparable to those needed to cause bleaching. I further show that these parameters are sensitive to pathogen stress as well. In several case studies of diseased and thermally stressed corals, I demonstrate that these lipid biomarkers of coral stress may be applied to zooxanthellae isolated from environmental samples. I show that these same compounds are preserved within coral aragonite, which opens up the potential to retrieve lipid-­‐based historical records of coral health from annual layers of coral skeleton. This work demonstrates the value of using lipid biomarkers to assess coral health and better understand the biochemical mechanisms of coral bleaching.This work was supported by a grant from the Summit Foundation, Award No. USA 00002/KSA 00011 made by King Abdullah University of Science and Technology (KAUST), and funding from the Woods Hole Oceanographic Institution

Lipid biomarkers of coral stress : calibration and exploration

Thesis (Ph. D.)--Joint Program in Oceanography/Applied Ocean Science and Engineering (Massachusetts Institute of Technology, Dept. of Earth, Atmospheric, and Planetary Sciences; and the Woods Hole Oceanographic Institution), 2011.Cataloged from PDF version of thesis.Includes bibliographical references.Corals are increasingly threatened by warming sea surface temperatures and other anthropogenic changes. The delicate symbiosis between corals and their algal endosymbionts (zooxanthellae) is easily disrupted by thermal stress, leading to bleaching and eventual mortality. The use of lipid ratios as biomarkers of environmental conditions is well established. Coral biomass contains abundant lipids, and the potential of lipid parameters to diagnose thermal tolerance in zooxanthellae has been previously suggested. In this thesis, I explore the response of specific fatty acids, sterols, and thylakoid membrane lipids to thermal and disease stress in zooxanthellae grown in culture, as well as those isolated from living corals. I present the discovery of a bioactive thylakoid lipid within zooxanthellae cells, and show how this compound is selectively mobilized in thermally stressed cells. I present a plausible mechanism for the breakdown of this compound into products that may cause apoptosis and disrupt the coral-algal symbiosis, eventually causing bleaching. I present two new lipid biomarkers of thermal stress in zooxanthellae, the C18 fatty acid unsaturation ratio, and the fatty acid to sterol ratio. I calibrate the decline of these two parameters to levels of thermal stress comparable to those needed to cause bleaching. I further show that these parameters are sensitive to pathogen stress as well. In several case studies of diseased and thermally stressed corals, I demonstrate that these lipid biomarkers of coral stress may be applied to zooxanthellae isolated from environmental samples. I show that these same compounds are preserved within coral aragonite, which opens up the potential to retrieve lipid-based historical records of coral health from annual layers of coral skeleton. This work demonstrates the value of using lipid biomarkers to assess coral health and better understand the biochemical mechanisms of coral bleaching.by Jessie Mary Kneeland.Ph.D

Alkenone-based evidence of Holocene slopewater cooling in the northwest Atlantic

Thesis (S.M.)--Massachusetts Institute of Technology, Dept. of Earth, Atmospheric, and Planetary Sciences, 2006.Includes bibliographical references (p. 85-89).Alkenone-based estimates of sea surface temperature (SST) in the northwest Atlantic during the last 10,000 years are presented and used to assess scenarios for Holocene climate variability. Alkenone concentration and unsaturation records are presented from cores KNR140-39GGC, KNR140-51GGC, MD95-2028, MD95-2031, and MD95-2025 from the Blake Ridge (320N), Carolina Slope (330N), Fogo Seamount (42°N), Narwhal (440N), and Orphan Basin (500N) respectively. The southernmost core, from the Blake Ridge, indicates very little temperature variation over the Holocene. Somewhat inshore and to the north of that location, the Carolina Slope record shows a slight cooling trend of about 1.50C over the past 5,000 years, which is interrupted by a brief but sudden drop of about 1C between 3,000 and 2,000 years before present. Lack of age control for the core from Fogo Seamount prevents any conclusions about the time frame of alkenone variation at that location. At the Narwhal site, which is not far from the Laurentian fan, a strong and consistent cooling of 9C is the most recent pattern of variation. Alkenone concentrations from the Orphan Basin were not sufficient for reliable measurement of a Holocene temperature trend.(cont.) The general pattern of strong cooling in the northern slope water region and very modest cooling south of Cape Hatteras, where the Gulf Stream separates from the coastline and heads out. to sea, may suggest a shift in mean Gulf Stream path as a possible culprit for the temperature record seen at the Narwhal site. However, changes of incoming solar radiation or seasonality of alkenone production over the Holocene provide alternative mechanisms for alkenone temperature variation.by Jessie M. Kneeland.S.M

Lipid biomarkers in Symbiodinium dinoflagellates : new indicators of thermal stress

Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution. The definitive version was published in Coral Reefs 32 (2013): 923-934, doi:10.1007/s00338-013-1076-3.Lipid content and fatty acid profiles of corals and their dinoflagellate endosymbionts are known to vary in response to high temperature stress. To better understand the heat stress response in these symbionts, we investigated cultures of Symbiodinium goreauii type C1 and Symbiodinium clade subtype D1 grown under a range of temperatures and durations. The predominant lipids produced by Symbiodinium are palmitic (C16) and stearic (C18) saturated fatty acids and their unsaturated analogs, docosahexaenoic (C22:6, n-3) polyunsaturated fatty acid (PUFA), and a variety of sterols. The relative amount of unsaturated acids within the C18 fatty acids in Symbiodinium tissue decreases in response to thermal stress. Prolonged exposure to high temperature also causes a decrease in abundance of fatty acids relative to sterols. These shifts in fatty acids and sterols are common to both types C1 and D1, but the apparent thermal threshold of lipid changes is lower for type C1. This work indicates that ratios among free fatty acids and sterols in Symbiodinium can be used as sensitive indicators of thermal stress. If the Symbdionium lipid stress response is unchanged in hospite, the algal heat stress biomarkers we have identified could be measured to detect thermal stress within the coral holobiont.. These results provide new insights into the potential role of lipids in the overall Symbiodinium thermal stress response.This research was supported by Award No. USA 00002 to K. Hughen made by King Abdullah University of Science and Technology (KAUST).2014-12-0