Planktonic Lipidome Responses to Aeolian Dust Input in Low-Biomass Oligotrophic Marine Mesocosms

Abstract

The effect and fate of dry atmospheric deposition on nutrient-starved plankton in the Eastern Mediterranean Sea (EMS; Crete, 2012) was tested by spiking oligotrophic surface seawater mesocosms (3 m 3 ) with Saharan dust (SD; 1.6 g L −1 ; 23 nmol NO x mg −1 ; 2.4 nmol PO 4 mg −1 ) or mixed aerosols (A; 1.0 g L −1 ; 54 nmol NO x mg −1 ; 3.0 nmol PO 4 mg −1 ) collected from natural and anthropogenic sources. Using high resolution liquid chromatography-mass spectrometry, the concentrations of over 350 individual lipids were measured in suspended particles to track variations in the lipidome associated with dust fertilization. Bacterial and eukaryotic intact polar lipid (IPL) biomarkers were categorized into 15 lipid classes based on headgroup identity, including four novel IPL headgroups. Bulk IPL concentrations and archaeal tetraether lipids were uncoupled with the doubling of chlorophyll concentrations that defined the stimulation response of oligotrophic plankton to SD or A amendment. However, molecular level analysis revealed the dynamics of the IPL pool, with significant additions or losses of specific IPLs following dust spikes that were consistent among treatment mesocosms. Multivariate redundancy analysis further demonstrated that the distribution of IPL headgroups and molecular modifications within their alkyl chains were strongly correlated with the temporal evolution of the plankton community and cycling of phosphate. IPLs with phosphatidylcholine, betaine, and an alkylamine-like headgroup increased in the post-stimulated period, when phosphate turnover time had decreased by an order of magnitude and phosphorus uptake was dominated by plankton >2 µm. For most IPL classes, spiking with SD or A yielded significant increases in the length and unsaturation of alkyl chains. A lack of corresponding shifts in the plankton community suggests that the biosynthesis of nitrogenous and phosphatidyl lipids may respond to physiological controls during episodic additions of dust to the EMS. Furthermore, alkyl chain distributions of IPLs containing N, P, and S invoked a bacterial source, suggesting that bacterioplankton are able to modulate these lipids in response to nutrient stress.

Phospholipid turnover rates suggest that bacterial community growth rates in the open ocean are systematically underestimated

“…We applied Eq. 4 to measure the turnover rates of PG and PE, which are derived primarily from marine heterotrophic bacterial communities (Van Mooy et al 2009;Popendorf et al 2011;Kharbush et al 2016;Meador et al 2017). Measurements were performed during five research cruises to the Sargasso Sea, the temperate western North Atlantic, and the subtropical North and South Pacific (Fig.…”

“…However, the technique was never widely applied in the upper ocean, presumably because phytoplankton also take up phosphate and the analytical methods necessary to identify the primary sources of specific phospholipids in the upper ocean were not yet readily available. Through advances in geochemical and microbial analytical techniques, multiple lines of evidence now show that two classes of phospholipids, phosphatidylglycerol (PG), and phosphatidylethanolamine (PE) are derived primarily from heterotrophic bacteria in the open ocean, opening the door for using these molecules to evaluate bacterial community growth dynamics (Van Mooy et al 2009;Van Mooy and Fredricks 2010;Popendorf et al 2011;Kharbush et al 2016;Meador et al 2017). We combined previously published approaches to determine biosynthesis rates (Van Mooy et al 2014) and concentrations (Popendorf et al 2013) of PG and PE to calculate the steady-state turnover rates of these molecules.…”

Desert dust deposition supplies essential bioelements to Red Sea corals

“…and a bacteria capable of solubilizing Fe (Basu et al, 2019). Finally, changes in bacterial lipid composition (Meador et al, 2017) or in zooplankton and picoplankton community composition (Feliú et al, 2020; Wu et al, 2018) were recorded after dust addition.…”

Lipid remodeling in phytoplankton exposed to multi-environmental drivers in a mesocosm experiment

“…The remodeling of intact polar lipids (IPLs), the main constituents of cell and chloroplast membranes, provides numerous physiological adjustments to attenuate environmental stressors impacting phytoplankton (Zienkiewicz et al, 2016;Du and Benning 2016;Morales et al, 2021). These include nutrient limitation (Van Mooy et al, 2009;Meador et al, 2017;Abida et al, 2015;Urzica et al, 2013;Gordillo et al, 1998;Wang et al, 2016), homeoviscous regulation in response to changing temperature (Sato et al, 1979;Wada and Murata, 1990;Sinensky, 1974;Neidleman, 1987;Tatsusawa and Takizawa 1996) and pH (Tatsusawa and Takizawa 1996;Poerschmann et al, 2004;Guckert and Cooksey, 1990), or photosynthetic function under varying light availability (Sato et al, 2003;Gombos et al, 2002;Pineau et al, 2004;Simionato et al, 2013;Gašparović et al, 2013;Khotimchenko and Yakovleva, 2005). While IPL distributions in environmental studies are typically used as chemotaxonomic biomarkers that trace the presence and abundance of specific microbial groups (Sturt et al, 2004;Schubotz et al, 2009;Van Mooy and Fredricks, 2010), their distributions have been used to in conjunction with additional microbial or geochemical measurements to assess how microbial metabolisms contribute to the chemical environment (Van Mooy et al, 2009;Wakeham et al, 2012;Schubotz et al, 2018;Cantarero et al, 2020).…”