Trace Metal Availability for Alkaline Phosphatases: A Proteomic Perspective from the Oligotrophic North Atlantic

Korinna Kunde, University of Southampton, Ocean and Earth Science, Southampton, United Kingdom, Noelle Held, Woods Hole Oceanographic Institution, Woods Hole, MA, United States, Clare Davis, University of Hawaii, School of Ocean and Earth Science and Technology, United States, Neil Wyatt, University of Southampton, United Kingdom, Matthew R McIlvin, Woods Hole Oceanographic Institution, Marine Chemistry and Geochemistry, Woods Hole, United States, Malcolm Woodward, Plymouth Marine Laboratory, Plymouth, United Kingdom, Mak A Saito, Woods Hole Oceanographic Institution, Marine Chemistry & Geochemistry, Woods Hole, United States, Alessandro Tagliabue, University of Liverpool, Department of Earth, Ocean and Ecological Sciences, Liverpool, United Kingdom, Claire Mahaffey, University of Liverpool, Earth, Ocean and Ecological Sciences, Liverpool, United Kingdom and Maeve C Lohan, University of Southampton, Ocean and Earth Sciences, National Oceanography Centre, Southampton, United Kingdom
Abstract:
Chronically low inorganic phosphate concentrations are characteristic of the oligotrophic subtropical North Atlantic and can limit primary production and nitrogen fixation. Dissolved organic phosphorus (DOP) provides a crucial alternative source of phosphorus for microbes via enzyme-mediated hydrolysis. Alkaline phosphatases (AP) cleave phosphate from ester moieties, the major component of DOP. Due to the dependence of AP on the trace metals zinc (Zn), cobalt (Co) or iron (Fe) as co-factors, we hypothesised a metal-phosphorus co-limitation of biological activity.

To test this, we conducted large volume incubations (24L) over 48h with additions of Zn, Co or Fe along strong biogeochemical gradients at 22°N in summer 2017. We employed absolute quantitative proteomics to measure the concentrations of AP of the important primary producers Synechococcus and Prochlorococcus, detecting changes at the cellular level. We observed two opposing responses with an increase in the Synechococcus Zn/Co-dependent AP upon Zn and Co additions in the Sargasso Sea and an increase in the Prochlorococcus Fe-dependent AP upon Fe addition in the eastern subtropical basin. Our results suggest that AP and hence DOP acquisition were reduced by metal availability at some locations, but the specifics of limitation in terms of responsive organism, AP type and metal stimulation were distinctive depending on the biogeochemical setting of the given locale, i.e. community structure, phosphorus nutritional status and metal concentrations. Furthermore, AP concentrations of the two primary producers were on the same order of magnitude despite a ~15-fold higher cell abundance of Prochlorococcus, suggesting that DOP acquisition via AP is more significant for Synechococcus to reach their cellular phosphorus demands.

Our findings demonstrate the complexity of phosphorus limitation in the oligotrophic North Atlantic and have important implications in the light of global change and the projected alteration of biogeochemical cycles.

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