Holm
Henry C.
Holm
Henry C.
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ArticleCoordinated transformation of the gut microbiome and lipidome of bowhead whales provides novel insights into digestion(Springer Nature, 2019-12-02) Miller, Carolyn A. ; Holm, Henry C. ; Horstmann, Lara ; George, John C. ; Fredricks, Helen F. ; Van Mooy, Benjamin A. S. ; Apprill, AmyWhale digestion plays an integral role in many ocean ecosystems. By digesting enormous quantities of lipid-rich prey, whales support their energy intensive lifestyle, but also excrete nutrients important to ocean biogeochemical cycles. Nevertheless, whale digestion is poorly understood. Gastrointestinal microorganisms play a significant role in vertebrate digestion, but few studies have examined them in whales. To investigate digestion of lipids, and the potential contribution of microbes to lipid digestion in whales, we characterized lipid composition (lipidomes) and bacterial communities (microbiotas) in 126 digesta samples collected throughout the gastrointestinal tracts of 38 bowhead whales (Balaena mysticetus) harvested by Alaskan Eskimos. Lipidomes and microbiotas were strongly correlated throughout the gastrointestinal tract. Lipidomes and microbiotas were most variable in the small intestine and most similar in the large intestine, where microbiota richness was greatest. Our results suggest digestion of wax esters, the primary lipids in B. mysticetus prey representing more than 80% of total dietary lipids, occurred in the mid- to distal small intestine and was correlated with specific microorganisms. Because wax esters are difficult to digest by other marine vertebrates and constitute a large reservoir of carbon in the ocean, our results further elucidate the essential roles that whales and their gastrointestinal microbiotas play in the biogeochemical cycling of carbon and nutrients in high-latitude seas.
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ArticleMicrobial ecology of coral-dominated reefs in the Federated States of Micronesia(Inter Research, 2021-04-22) Apprill, Amy ; Holm, Henry C. ; Santoro, Alyson E. ; Becker, Cynthia ; Neave, Matthew J. ; Hughen, Konrad A. ; Richards Donà, Angela ; Aeby, Greta S. ; Work, Thierry M. ; Weber, Laura ; McNally, SeanMicroorganisms are central to the functioning of coral reef ecosystems, but their dynamics are unstudied on most reefs. We examined the microbial ecology of shallow reefs within the Federated States of Micronesia. We surveyed 20 reefs surrounding 7 islands and atolls (Yap, Woleai, Olimarao, Kosrae, Kapingamarangi, Nukuoro, and Pohnpei), spanning 875053 km2. On the reefs, we found consistently higher coral coverage (mean ± SD = 36.9 ± 22.2%; max 77%) compared to macroalgae coverage (15.2 ± 15.5%; max 58%), and low abundances of fish. Reef waters had low inorganic nutrient concentrations and were dominated by Synechococcus, Prochlorococcus, and SAR11 bacteria. The richness of bacterial and archaeal communities was significantly related to interactions between island/atoll and depth. High coral coverage on reefs was linked to higher relative abundances of Flavobacteriaceae, Leisingera, Owenweeksia, Vibrio, and the OM27 clade, as well as other heterotrophic bacterial groups, consistent with communities residing in waters near corals and within coral mucus. Microbial community structure at reef depth was significantly correlated with geographic distance, suggesting that island biogeography influences reef microbial communities. Reefs at Kosrae Island, which hosted the highest coral abundance and diversity, were unique compared to other locations; seawater from Kosrae reefs had the lowest organic carbon (59.8-67.9 µM), highest organic nitrogen (4.5-5.3 µM), and harbored consistent microbial communities (>85% similar), which were dominated by heterotrophic cells. This study suggests that the reef-water microbial ecology on Micronesian reefs is influenced by the density and diversity of corals as well as other biogeographical features.
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ThesisMicrobial glycerolipids in the global ocean: environmental controls and sinking flux dynamics(Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, 2024-02) Holm, Henry C. ; Van Mooy, Benjamin A. S.The composition of glycerolipids from a range of ocean environments were analyzed to better understand the biochemical adaptations and remineralization processes of planktonic biomass. Glycerolipids compose the cell membranes and energy stores of ocean microorganisms. As a biochemical group they present a useful target for tracking a wide range of environmental stress responses. In Chapter 2 of this work, I employ high resolution mass spectrometry to assemble a global dataset of planktonic lipidomes. Using this dataset of samples mostly from the epipelagic, I find that water temperature is a major controlling factor on fatty acid saturation state and hypothesize this derives from known biophysical constraints on cell membranes. I extend this analysis further to investigate links between long-chain essential fatty acids (LCEFA) and temperature. My analysis shows that the abundance of one of these LCEFAs (eicosapentaenoic acid, 20:5 n-3) is well correlated with temperature. Using this relationship, I project temperature-based declines in its abundance due to climate change over the next century. In Chapter 3, using samples from the West Antarctic peninsula, I assess the pigments and glycerolipid compositions of microbial communities within seasonal pack ice floes to gain insights on growth in an extremophile environment. The caloric content of this glycerolipid biomass is additionally calculated to assess its value to higher trophic level consumers within the sea ice ecosystem. I find that glycerolipids’ physical distribution within sea ice core to be calorically dense but highly geographically and physically heterogenous. I additionally show evidence of a new biomarker (fatty acid hydroxy fatty acid triacylglycerols, FAHFA-TAG) which have not been detected before in an ocean system. I further evaluate the possible biochemical sources of these novel biomarkers within sea ice. Lastly, I examine the glycerolipids present in sinking material from two separate studies of carbon flux in the upper mesopelagic. These compositions revealed both sources and remineralization processes influencing lipid carbon. I find evidence that lipid biomass is mostly lost non-selectively from particles, differing from previous reports of selective degradation of lipids. However, I find compositional differences between surface-suspended and sinking material possibly pointing to selection mechanisms at sinking material conception. I use glycerolipids to create a new source metric predicting the relative amounts of sinking material derived from fecal pellets verse aggregates. The findings of this thesis extend our understanding of microbial biochemical adaptations to their environment and reveal controlling factors on glycerolipid cycling in the ocean system.