Microbial degradation of dissolved organic carbon (DOC) in aquatic environments can cause oxygen depletion, water acidification, and CO₂ emissions. These problems are caused by labile DOC (LDOC) and not refractory DOC (RDOC) that resists degradation and is thus a carbon sink. For nearly a century, chemical oxygen demand (COD) has been widely used for assessment of organic pollution in aquatic systems. Here, we show through a multicountry survey and experimental studies that COD is not an appropriate proxy of microbial degradability of organic matter because it oxidizes both LDOC and RDOC, and the latter contributes up to 90% of DOC in high-latitude forested areas. Hence, COD measurements do not provide appropriate scientific information on organic pollution in natural waters and can mislead environmental policies. We propose the replacement of the COD method with an optode-based biological oxygen demand method to accurately and efficiently assess organic pollution in natural aquatic environments.

Lipids are structurally diverse biomolecules that serve multiple roles in cells. As such, they are used as biomarkers in the modern ocean and as paleoproxies to explore the geological past. Here, I review lipid geochemistry, biosynthesis, and compartmentalization; the varied uses of lipids as biomarkers; and the evolution of analytical techniques used to measure and characterize lipids. Advancements in high-resolution accurate-mass mass spectrometry have revolutionized the lipidomic and metabolomic fields, both of which are quickly being integrated into marine meta-omic studies. Lipidomics allows us to analyze tens of thousands of features, providing an open analytical window and the ability to quantify unknown compounds that can be structurally elucidated later. However, lipidome annotation is not a trivial matter and represents one of the biggest challenges for oceanographers, owing in part to the lack of marine lipids in current in silico databases and data repositories. A case study reveals the gaps in our knowledge and open opportunities to answer fundamental questions about molecular-level control of chemical reactions and global-scale patterns in the lipidscape.

Ecophysiological stress and the grazing of diatoms are known to elicit the production of chemical defense compounds called oxylipins, which are toxic to a wide range of marine organisms. Here we show that (1) the viral infection and lysis of diatoms resulted in oxylipin production; (2) the suite of compounds produced depended on the diatom host and the infecting virus; and (3) the virus-mediated oxylipidome was distinct, in both magnitude and diversity, from oxylipins produced due to stress associated with the growth phase. We used high-resolution accurate-mass mass spectrometry to observe changes in the dissolved lipidome of diatom cells infected with viruses over 3 to 4 days, compared to diatom cells in exponential, stationary, and decline phases of growth. Three host virus pairs were used as model systems: Chaetoceros tenuissimus infected with CtenDNAV; C. tenuissimus infected with CtenRNAV; and Chaetoceros socialis infected with CsfrRNAV. Several of the compounds that were significantly overproduced during viral infection are known to decrease the reproductive success of copepods and interfere with microzooplankton grazing. Specifically, oxylipins associated with allelopathy towards zooplankton from the 6-, 9-, 11-, and 15-lipogenase (LOX) pathways were significantly more abundant during viral lysis. 9-hydroperoxy hexadecatetraenoic acid was identified as the strongest biomarker for the infection of Chaetoceros diatoms. C. tenuissimus produced longer, more oxidized oxylipins when lysed by CtenRNAV compared to CtenDNAV. However, CtenDNAV caused a more statistically significant response in the lipidome, producing more oxylipins from known diatom LOX pathways than CtenRNAV. A smaller set of compounds was significantly more abundant in stationary and declining C. tenuissimus and C. socialis controls. Two allelopathic oxylipins in the 15-LOX pathway and essential fatty acids, arachidonic acid (ARA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) were more abundant in the stationary phase than during the lysis of C. socialis. The host–virus pair comparisons underscore the species-level differences in oxylipin production and the value of screening more host–virus systems. We propose that the viral infection of diatoms elicits chemical defense via oxylipins which deters grazing with downstream trophic and biogeochemical effects.

Lipids are essential biomolecules for cell physiology and are commonly used as biomarkers to elucidate biogeochemical processes over a large range of environments and timescales. Here, we use high-temporal-resolution lipidomic analysis to characterize the surface ocean community in the productive upwelling region overlying the Monterey Bay Canyon. We observed a strong diel signal with a drawdown of lipids at night and an increase during the day that seemed to correspond to wholesale removal of lipids from the surface ocean as opposed to internal metabolism. Individual lipid species were organized into coregulated groups that were interpreted as representing different phytoplankton guilds. Concentrations of long-chained triacylglycerols (TAGs) showed unique patterns over the course of five days. TAGs were used to estimate the amount of energy cycled through the surface ocean. These calculations revealed diurnal carbon cycling that was on scales comparable to net primary production. The diel pattern dissipated from most lipid modules on Day 3 as tidal forcing increased at our site with the advent of the new moon. Pigment analysis indicated that the community shifted from a diatom-dominated community to a more diverse assemblage, including more haptophytes, chlorophytes, and Synechococcus during the new moon. The shift in community appears to promote higher nutritional quality of biomass, with more essential fatty acids in the surface ocean during the spring tide. This analysis showcases the utility of lipidomics in characterizing community dynamics and underscores the importance of considering both diel and tidal timescales when sampling in productive coastal regions.

/Summary: Diatoms are large phytoplankton that form the base of the marine food web and often bloom first when nutrients are injected into the surface ocean through upwelling or deep ocean mixing ^1,2 . Diatoms contribute 20% of global photosynthesis ³ while disproportionately representing 40% of carbon export ⁴ , with most export occurring along the continental margins ⁵ . Oxylipin chemical signaling by diatoms has been extensively studied in the Mediterranean Sea where oxylipins are linked to grazing with subsequent insidious effects on copepod reproduction ^6–13 . Culture studies with diatoms have shown that stress, growth phase, and viral infection also impact oxylipin production ^14–16 . This study provides insight into the role of oxylipins as biomarkers and chemical signals during viral infection of diatoms in natural communities. Biomarkers for lysis and senescence were identified in laboratory experiments and observed at elevated concentrations in meta-lipidomes collected in the California Coastal Ecosystem (CCE) where diatoms had recently been lysed by viruses ¹⁷ . Deck-board incubations with natural communities show that oxylipins stimulate sinking particle-attached and surface-ocean microbes in a dose and community-dependent manner, while inhibiting microzooplankton grazing and phytoplankton growth rates. Carbon export was two times higher at the Post-lytic site than elsewhere along the transect consistent with the viral shuttle, whereby viruses facilitate carbon export. We previously reported enhanced enzymatic activity at the Post-lytic site ¹⁷ , suggestive of the viral shunt, whereby carbon is remineralized or attenuated into non-sinking dissolved organic matter. Here we layer geochemical evidence to show that lysis of oxylipin producing diatoms amplified the vertical flux of carbon from the surface ocean even in the presence of viral shunt processes. The remineralization length scale and community composition have been hypothesized as controls on shunt vs. shuttle ^18–20; our analysis provides another example of how community interactions may toggle a system between favoring shunt or shuttle.

Marine diatoms are an important group of phytoplankton that can shape marine ecosystems and global carbon cycling. When stressed, either physiologically or by grazing, diatoms release oxidized, lipid-derived signals known as oxylipins. Diatom-derived oxylipins are proposed to serve as defense and signaling chemicals that affect multiple components of marine ecosystems. Therefore, to elucidate the diversity of diatom-derived oxylipins produced during stress, we profiled the spectrum of dissolved lipids of five diatom species in culture under silicon limitation and across growth phases using ultra-high performance liquid chromatography coupled with high-resolution accurate mass spectrometry. In this study, we present evidence that physiological changes associated with Si-limitation elicit the extracellular release of linear oxygenated fatty acids (LOFAs) across five diatom species. For diatoms like Skeletonema japonicum and Pseudo-nitzschia multiseries, silicon limitation induced a distinct lipidomic signature driven by oxylipins known to be allelopathic. While their lipoxygenases were found to be different, S. japonicum and P. multiseries had the most similar dissolved lipidomes, suggesting alternative controls on oxylipin biosynthesis. Consequently, elevated oxylipin concentrations with silicon stress, estimated up to 5.91 µM, pose implications for diatoms at sea, potentially affecting ecosystems and biogeochemistry.