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Abstract The daily cycle of solar radiation has a profound influence in structuring the physiology of microbes in the euphotic zone and subsequently setting the degree of coupling across trophic levels within ocean ecosystems. There has been an upsurge of interest in the biological role of the diel cycle and the ability to probe it using molecular approaches (i.e., “omics”), which now allow us to pinpoint the level of detail of the diel cycle that is required to better understand microbes' roles across multiple biogeochemical cycles. Although sampling the diel cycle requires additional resources, the payback is large. A better understanding of the diel cycle provides a holistic framework with which to align patterns and causal sequences across multi‐omic layers, yielding consequent connections with metabolic processes to develop more robust mechanistic models. Such models provide the stepping stones to better understand how resource allocation in cells is driven by environmental forcing. 

ABSTRACT Aerobic anoxygenic phototrophic (AAP) bacteria harvest light energy using bacteriochlorophyll-containing reaction centers to supplement their mostly heterotrophic metabolism. While their abundance and growth have been intensively studied in coastal environments, much less is known about their activity in oligotrophic open ocean regions. Therefore, we combinedin situsampling in the North Pacific Subtropical Gyre, north of O'ahu island, Hawaii, with two manipulation experiments. Infra-red epifluorescence microscopy documented that AAP bacteria represented approximately 2% of total bacteria in the euphotic zone with the maximum abundance in the upper 50 m. They conducted active photosynthetic electron transport with maximum rates up to 50 electrons per reaction center per second. Thein situdecline of bacteriochlorophyll concentration over the daylight period, an estimate of loss rates due to predation, indicated that the AAP bacteria in the upper 50 m of the water column turned over at rates of 0.75–0.90 d⁻¹. This corresponded well with the specific growth rate determined in dilution experiments where AAP bacteria grew at a rate 1.05 ± 0.09 d⁻¹. An amendment of inorganic nitrogen to obtain N:P = 32 resulted in a more than 10 times increase in AAP abundance over 6 days. The presented data document that AAP bacteria are an active part of the bacterioplankton community in the oligotrophic North Pacific Subtropical Gyre and that their growth was mostly controlled by nitrogen availability and grazing pressure.IMPORTANCEMarine bacteria represent a complex assembly of species with different physiology, metabolism, and substrate preferences. We focus on a specific functional group of marine bacteria called aerobic anoxygenic phototrophs. These photoheterotrophic organisms require organic carbon substrates for growth, but they can also supplement their metabolic needs with light energy captured by bacteriochlorophyll. These bacteria have been intensively studied in coastal regions, but rather less is known about their distribution, growth, and mortality in the oligotrophic open ocean. Therefore, we conducted a suite of measurements in the North Pacific Subtropical Gyre to determine the distribution of these organisms in the water column and their growth and mortality rates. A nutrient amendment experiment showed that aerobic anoxygenic phototrophs were limited by inorganic nitrogen. Despite this, they grew more rapidly than average heterotrophic bacteria, but their growth was balanced by intense grazing pressure. 

Microbial responses to environmental changes are well studied in laboratory cultures, but in situ adaptations of plankton lipidomes remain less understood. Building upon a global lipidomic study showing temperature-driven lipid unsaturation regulation in marine plankton, we expanded the analysis spatially and methodologically to investigate the in situ adaptations of marine plankton. Through weighted correlation network analysis of 3164 lipid species from 930 samples, we identified 16 structurally distinct lipid clusters co-occurred across diverse oceanographic conditions. The highest lipid diversity was observed in the polar oceans, where plankton uses chain shortening for cold acclimation. Conversely, in the surface of tropical and subtropical oceans, plankton showed enrichment in non-phosphorus lipids, likely responding to warm temperature, with potential implications for the elemental stoichiometry of the biological pump. In the subsurface of these regions, highly unsaturated lipids were enriched, suggesting phytoplankton adaptation to low light and contributing unsaturated fatty acids to tropical and subtropical ocean food webs. 

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. 

Climate-change-related declines in the availability of some essential fatty acids to marine food webs may affect future fisheries.