Using High-Sensitivity Lipidomics To Assess Microscale Heterogeneity in Oceanic Sinking Particles and Single Phytoplankton Cells

Abstract

Sinking particulate organic matter (POM) is a primary component of the ocean's biological carbon pump that is responsible for carbon export from the surface to the deep sea. Lipids derived from plankton comprise a significant fraction of sinking POM. Our understanding of planktonic lipid biosynthesis and the subsequent degradation of lipids in sinking POM is based on the analysis of bulk samples that combine many millions of plankton cells or dozens of sinking particles, which averages out natural heterogeneity. We developed and applied a nanoflow high-performance liquid-chromatography electrospray-ionization highresolution accurate-mass mass spectrometry lipidomic method to show that two types of sinking particlesmarine snow and fecal pelletscollected in the western North Atlantic Ocean have distinct lipidomes, providing new insights into their sources and degradation that would not be apparent from bulk samples. We pressed the limit of this approach by examining individual diatom cells from a single culture, finding marked lipid heterogeneity, possibly indicative of fundamental mechanisms underlying cell division. These single-cell data confirm that even cultures of phytoplankton cells should be viewed as mixtures of physiologically distinct populations. Overall, this work reveals previously hidden lipidomic heterogeneity in natural POM and phytoplankton cells, which may provide critical new insights into microscale chemical and microbial processes that control the export of sinking POM.

Microbial metabolic specificity controls pelagic lipid export efficiency

“…Lipidomic analysis. All lipidomic analysis was done according to a previously described method 21 . In short, nanoflow high-performance liquid-chromatography (nano-HPLC) was performed with a Thermo Scientific Easy nLC 1200 apparatus.…”

Molecular-level evidence of early lipid transformations throughout oceanic depths

“…Abiotic degradation of chlorophyll phytyl chain, carotenoids, D5-sterols, unsaturated fatty acids, alkenones, and unsaturated alkenes in the marine realm has also been investigated (Rontani and Belt, 2020 and references therein). Additional studies have focused on lipid degradation in the ocean water column (Wakeham et al, 1997a(Wakeham et al, , 1997b(Wakeham et al, , 2002Sheridan et al, 2002;Goutx et al, 2007;Collins et al, 2018;Hunter et al, 2021). Examining the photooxidation of intact polar lipids in surface waters of the West Antarctic Peninsula, Collins et al (2018) found that photooxidation occurs on a scale comparable to bacterial production and that significant rates of photooxidation are characteristic only of polyunsaturated fatty acids.…”

Toward a Multi-Omics-Based Single-Cell Environmental Chemistry and Toxicology

“…Analytical approaches for nanosamples can also be applied to single-particles. 7 Such approaches would also allow determining bioconcentration factors’ differences between different microorganisms or cells, which can efficiently be sorted with fluorescent, isotopic, or other probes. Eventually, the decrease of knowledge complexity that multiomics at single cell can offer, as a reductive approach to the system, will be invaluable within the adverse outcome pathway, which allows to relate cellular responses to environmental impacts.…”

“…So far, environmental studies on bioaccumulation or transformation of pollutants, or the effects of pollutants on organisms, tissues, or microorganisms has been based on bulk samples, but not on few cells (nanosamples). Such new age of knowledge at the cellular resolution, thanks to single-cell omics, is just starting to emerge in the environmental sciences. − …”

“…Hydrophobic pollutants accumulate in membranes with concentrations many orders of magnitude higher than in water, but the conceptual overcoming of the “hydrophobic paradigm”, where bioaccumulation is predicted by the octanol–water partition coefficient ( K OW ) or other physicochemical descriptors, may only be possible through multiomics at nanoscale, as there are detoxifying mechanisms modifying the ratio of internal/external concentrations, such as degradation and efflux pumps, that are intimately linked to the genes harbored by cells and their activation. Analytical approaches for nanosamples can also be applied to single-particles . Such approaches would also allow determining bioconcentration factors’ differences between different microorganisms or cells, which can efficiently be sorted with fluorescent, isotopic, or other probes.…”