Microbial metabolomics in polar oceans: responses to temperature and salinity changes associated with sea ice.
Abstract
Polar oceans and sea ice are among Earth’s major biomes, but are experiencing rapid environmental changes associated with climate change that may shift polar marine ecosystems into new, potentially unstable, states. Warming temperatures, alterations in sea-ice dynamics, and enhanced glacial freshwater input into coastal regions at the poles all stand to alter the temperature and salinity seascapes of an environment already marked by pronounced seasonal fluctuations. This dissertation examines the role of temperature and salinity change associated with sea-ice formation and melt in structuring the chemical inventory of organic matter in microbially dominated polar systems, with a focus on sea-ice algae. Much of this work utilizes liquid chromatography-mass spectrometry (LC-MS) to observe pools of small biomolecules (metabolites) that can serve as currencies of microbial metabolism and provide a snapshot of cellular activity. Specifically, I focus on gaps in our knowledge regarding protective compounds that are temperature- and salinity-sensitive (compatible solutes), many of which are highly labile metabolites with the capacity to fuel the microbial loop upon their release from cells. Chapter 1 introduces sea-ice microbial communities and the cellular strategies they use to grapple with the temperature and salinity fluctuations that characterize polar marine habitats. In Chapters 2 and 3, I examine the covarying impact of temperature and salinity on compatible solutes in the sea-ice diatom Nitzschia lecointei (Chapter 2) and analyze organic metabolite pools across cultured diatom species (Chapter 3). These chapters reveal that sea-ice algae can contain diverse and species-specific suites of labile compatible solutes at high concentrations (up to ~1 M; Chapter 3) with complex and varying cellular sensitivities to temperature and salinity change (Chapter 2), whereby the solutes are strongly accumulated under cold and salty conditions compared to warmer and fresher conditions. In Chapter 2 I also offer some of the first observations of multiple metabolites in natural Arctic sea ice and hypothesize on their impacts on the cycling of nutrients through this environment. In Chapter 4, I explore whole community metabolomes paired with environmental sequencing of 18S and 16S rRNA genes in distinct but interconnected Antarctic marine habitats (sea-ice meltwater, seawater, and sea ice) with unique physicochemical settings, including temperature and salinity. This chapter reveals unique communities in each habitat, all distinguishable by metabolomics. Chapter 4 also presents short-term experiments on natural microbial communities in polar seawater incubated under different temperature and salinity conditions mimicking sea-ice formation and melt, which demonstrated strong, community-wide metabolome reorganization, including alterations to the pools of numerous compatible solutes, but in the absence of corresponding community composition change. In full, this dissertation provides some of the first metabolite measurements in polar marine environments, identifies and explores the roles of key metabolites in microbial adaptation to environmental change, and provides a unique, metabolite-centered perspective on the potential impacts of continued environmental change on the production and use of organic matter in polar food webs and on the detection of life in icy environments beyond the Earth.
Collections
- Oceanography [134]