Biology subjects

Ingalls, A. E.

Publications and source records attributed to Ingalls, A. E..

5 recordsLinked to original sources

bioRxiv2021

Diverse arsenic-containing lipids in the surface ocean

Arsenic is present at nanomolar levels throughout the surface ocean, and microbes assimilate this toxic element due to its similarity to inorganic phosphorus. Although the concentration and characterization of dissolved arsenic has been a focus of ocean studies, the size of the particulate arsenic pool and its partitioning into organic molecules within the microbial community is not known. We measured the particulate pool of arsenic in five surface samples from the open ocean and determined the contribution of arsenic-containing lipids to this pool. Here we show that the accumulation of arsenic into lipids is a widespread phenomenon in the surface ocean. Particulate arsenic concentrations were 15 to 42 pmol L-1 with 7-20% of the particulate arsenic pool in the form of arsenolipids. We characterized these arsenolipids and found that arsenosugar phospholipids dominated the arsenolipid pools in our samples with a minor component of arsenohydrocarbons and other unidentified lipids. A significant portion of the arsenosugar phospholipids (up to 35%) were present as previously undescribed mixed acyl ether lipids, suggesting a bacterial source. Scientific significance statementMarine microbes experience constant exposure to the toxic element arsenic. However, there are no baseline measurements of how much arsenic accumulates in microbial communities nor do we know the full spectrum of arsenic containing biomolecules produced in marine systems. In culture-based studies there is strong evidence that phytoplankton synthesize arsenic-containing lipids, but these lipids have not been observed in natural communities of marine microbes. Here we make measurements of bulk particulate arsenic at five sites in the surface open ocean and show that a significant portion of this particulate arsenic is present as complex arsenic-containing lipids. We characterize this arsenolipid pool chemically and quantitatively to show a variety of chemically distinct and quantitatively significant lipids that expand our understanding of marine arsenic biogeochemistry. Data availability statementMass spectrometry data and its associated metadata will be available on Dryad with publication. Scripts for data processing and figure generation found on github at https://github.com/kheal/particulate_As_data_analysis.

ecology↗

bioRxiv2020

Marine community metabolomes carry fingerprints of phytoplankton community composition

Phytoplankton transform inorganic carbon into thousands of biomolecules that represent an important pool of fixed carbon, nitrogen, and sulfur in the surface ocean. Metabolite production differs between phytoplankton, and the flux of these molecules through the microbial food web depends on compound-specific bioavailability to members of a wider microbial community. Yet relatively little is known about the diversity or concentration of metabolites within marine plankton. Here we compare 313 polar metabolites in 21 cultured phytoplankton species and in natural planktonic communities across environmental gradients to show that bulk community metabolomes reflect chemical composition of the phytoplankton community. We also show that groups of compounds have similar patterns across space and taxonomy suggesting that the concentrations of these compounds in the environment are controlled by similar sources and sinks. We quantify several compounds in the surface ocean that represent substantial understudied pools of labile carbon. For example, the N-containing metabolite homarine was up to 3% of particulate carbon and is produced in high concentrations by cultured Synechococcus, and S-containing gonyol accumulated up to 2.5 nM in surface particles and likely originates from dinoflagellates. Our results show that phytoplankton composition directly shapes the carbon composition of the surface ocean. Our findings suggest that in order to access these pools of bioavailable carbon, the wider microbial community must be adapted to phytoplankton community composition. IMPORTANCEMicroscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet, the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Here we explore the abundance and diversity of small biomolecules in planktonic communities across ecological gradients in the North Pacific and within 21 cultured phytoplankton species. Our work demonstrates that phytoplankton diversity is an important determinant of the chemical composition of the highly bioavailable pool of organic carbon in the ocean, and we highlight understudied yet abundant compounds in both the environment and cultured organisms. These findings add to understanding of how the chemical makeup of phytoplankton shapes marine microbial communities where the ability to sense and use biomolecules depends on the chemical structure.

ecology↗

bioRxiv2020

Prochlorococcus extracellular vesicles: Molecular composition and adsorption to diverse microbes

Extracellular vesicles are small (~50-200 nm diameter) membrane-bound structures released by cells from all domains of life. While vesicles are abundant in the oceans, our understanding of their functions, both for cells themselves and the emergent ecosystem, is in its infancy. To advance this understanding, we analyzed the lipid, protein, and metabolite content of vesicles produced by the marine cyanobacterium Prochlorococcus. We show that Prochlorococcus exports an enormous array of cellular compounds into the surrounding seawater within vesicles. Vesicles produced by two different strains contain some materials in common, but also display numerous strain-specific differences, reflecting functional complexity within natural vesicle populations. Prochlorococcus vesicles contain active enzymes, indicating that they can mediate extracellular biogeochemical reactions in the ocean. We demonstrate that vesicles from Prochlorococcus and other bacteria associate with diverse microbes including the most abundant marine bacterium, Pelagibacter. Our observations suggest that vesicles may play diverse functional roles in the oceans, including but not limited to mediating energy and nutrient transfers, catalyzing extracellular biochemical reactions, and mitigating toxicity of reactive oxygen species. These findings indicate that a portion of dissolved compounds in the oceans are not truly dissolved, but are instead packaged within locally structured, particulate vesicles.

microbiology↗

bioRxiv2020

Community-scale Synchronization and Temporal Partitioning of Gene Expression, Metabolism, and Lipid Biosynthesis in Oligotrophic Ocean Surface Waters

Sunlight drives daily rhythms of photosynthesis, growth, and division of photoautotrophs throughout the surface oceans. However, the cascading impacts of oscillatory light input on diverse microbial communities and community-scale metabolism remains unclear. Here we use an unsupervised machine learning approach to show that a small number of diel archetypes can explain pervasive periodic dynamics amongst more than 65,000 distinct time series, including transcriptional activity, macromolecules, lipids, and metabolites from the North Pacific Subtropical Gyre. Overall, we find evidence for synchronous timing of carbon-cycle gene expression that underlie daily oscillations in the concentrations of particulate organic carbon. In contrast, we find evidence of asynchronous timing in gene transcription related to nitrogen metabolism and related metabolic processes consistent with temporal niche partitioning amongst microorganisms in the bacterial and eukaryotic domains.

ecology↗

bioRxiv2020

Diel Oscillations of Particulate Metabolites Reflect Synchronized Microbial Activity in the North Pacific Subtropical Gyre

Light is the primary input of energy into the sunlit ocean, driving daily oscillations in metabolism of primary producers. The consequences of this solar forcing have implications for the whole microbial community, yet in situ measurements of metabolites, direct products of cellular activity, over the diel cycle are scarce. We evaluated community-level biochemical consequences of diel oscillations in the North Pacific Subtropical Gyre by quantifying 79 metabolites in particulate organic matter in surface waters every four hours over eight days. Total particulate metabolite concentration peaked at dusk, even when normalized to biomass estimates. The concentrations of 70% of individual metabolites exhibited 24-hour periodicity. Despite the diverse organisms that use them, primary metabolites involved in anabolic processes and redox maintenance had significant 24-hour periodicity. Osmolytes exhibited the largest diel oscillations, implying rapid turnover and metabolic roles beyond cell turgor maintenance. Metatranscriptome analysis revealed the taxa involved in production and consumption of some metabolites, including the osmolyte trehalose. This compound displayed the largest diel oscillations in abundance and was likely produced by the nitrogen-fixing cyanobacterium Crocosphaera for energy storage. These findings demonstrate that paired measurements of particulate metabolites and transcripts resolve strategies microbes use to manage daily energy and redox oscillations.

ecology↗