High CO₂ concentration and iron availability determine the metabolic inventory in an Emiliania huxleyi‐dominated phytoplankton community

Abstract

Ocean acidification (OA), a consequence of anthropogenic carbon dioxide (CO 2) emissions, strongly impacts marine ecosystems. OA also influences iron (Fe) solubility, affecting biogeochemical and ecological processes. We investigated the interactive effects of CO 2 and Fe availability on the metabolome response of a natural phytoplankton community. Using mesocosms we exposed phytoplankton to ambient (390 μatm) or future CO 2 levels predicted for the year 2100 (900 μatm), combined with ambient (4.5 nM) or high (12 nM) dissolved iron (dFe). By integrating over the whole phytoplankton community, we assigned functional changes based on altered metabolite concentrations. Our study revealed the complexity of phytoplankton metabolism. Metabolic profiles showed three stages in response to treatments and phytoplankton dynamics. Metabolome changes were related to the plankton group contributing respective metabolites, explaining bloom decline and community succession. CO 2 and Fe affected metabolic profiles. Most saccharides, fatty acids, amino acids and many sterols significantly correlated with the high dFe treatment at ambient pCO 2. High CO 2 lowered the abundance of many metabolites irrespective of Fe. However, sugar alcohols accumulated, indicating potential stress. We demonstrate that not only altered species composition but also changes in the metabolic landscape affecting the plankton community may change as a consequence of future high-CO 2 oceans.

Ocean alkalinity enhancement using sodium carbonate salts does not impact Fe dynamics in a mesocosm experiment

“…In this experiment, both low pH and strong organic ligands enhanced the solubility of particulate and colloidal Fe (Segovia et al, 2017;. This promoted a significant higher Fe availability to phytoplankton, directly impacting on their physiology and controlling the phytoplankton community structure in coastal ecosystems (Segovia et al, 2017;Lorenzo et al, 2020;Mausz et al, 2020).…”

High-CO2 Levels Rather than Acidification Restrict Emiliania huxleyi Growth and Performance

“…It is now known that the different strains of E. huxleyi show phenotypic plasticity regarding their growth performance, light-responses, calcification, and virus susceptibility [ 14 ]. This phenomenon is most likely a consequence of genomic differences, transcriptomic [ 14 ], and metabolomic [ 15 ] responses to environmental conditions, and/or threats such as viral infections [ 60 ]. Moreover, methodological differences are also responsible for the variety of response patterns observed in growth and photosynthetic performance, as well as in calcification [ 24 , 29 ].…”

“…The presence of high levels of CO 2 did not only prevent cell division but also promoted the unviability of already formed cells [ 23 ]. It also affected the cellular level of many metabolites (175 out of 333 metabolites identified, [ 15 ]). All aminoacids (except glycine) and all detected TCA cycle substrates decreased at high CO 2 relative to control conditions.…”

“…E. huxleyi has a pangenome that provides this species with a high genome variability [ 14 ]. This is reflected in a plethora of alternative metabolic traits, a consequence of the ample metabolic repertoire displayed [ 14 , 15 ]. Such genome variability underpins its capacity to thrive in habitats ranging from the equator to the subarctic, forming extensive blooms under a large variety of environmental conditions that can be seen from outer space [ 14 , 16 ].…”

“…The response of E. huxleyi to carbonate chemistry variations has been studied both in the field using natural populations and in the laboratory using monocultures [ 7 , 17 – 21 ]. When exposed to elevated CO 2 and concomitantly low pH, E. huxleyi reduced its growth rate and its level of calcification in most of the experiments, leading to thinner coccospheres [ 22 ] and thus, imposing high stress to the cells that compromises their viability [ 15 , 23 ]. However, there is still controversy on whether OA will promote or reduce calcification rates, since some experiments with this same species have resulted in conflicting responses [ 19 , 22 , 24 – 26 ].…”