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Regulation of the Phytoplankton Heme B Iron Pool During the North Atlantic Spring Bloom Evangelia Louropoulou, Martha Gledhill, Thomas Browning, Dhwani K

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Regulation of the Phytoplankton Heme B Iron Pool During the North Atlantic Spring Bloom Evangelia Louropoulou, Martha Gledhill, Thomas Browning, Dhwani K Regulation of the Phytoplankton Heme b Iron Pool During the North Atlantic Spring Bloom Evangelia Louropoulou, Martha Gledhill, Thomas Browning, Dhwani K. Desai, Jan-Lukas Menzel Barraqueta, Manon Tonnard, Géraldine Sarthou, Hélène Planquette, Andrew Bowie, Ruth Schmitz, et al. To cite this version: Evangelia Louropoulou, Martha Gledhill, Thomas Browning, Dhwani K. Desai, Jan-Lukas Menzel Bar- raqueta, et al.. Regulation of the Phytoplankton Heme b Iron Pool During the North Atlantic Spring Bloom. Frontiers in Microbiology, Frontiers Media, 2019, 10, pp.1566. 10.3389/fmicb.2019.01566. hal-02322547 HAL Id: hal-02322547 https://hal.archives-ouvertes.fr/hal-02322547 Submitted on 16 Jun 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. fmicb-10-01566 July 11, 2019 Time: 12:11 # 1 ORIGINAL RESEARCH published: 11 July 2019 doi: 10.3389/fmicb.2019.01566 Regulation of the Phytoplankton Heme b Iron Pool During the North Atlantic Spring Bloom Evangelia Louropoulou1,2*, Martha Gledhill1, Thomas J. Browning1, Dhwani K. Desai3, Jan-Lukas Menzel Barraqueta1,4, Manon Tonnard5,6,7, Géraldine Sarthou5, Hélène Planquette5, Andrew R. Bowie6,7, Ruth A. Schmitz2, Julie LaRoche3 and Eric P. Achterberg1 1 GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany, 2 Institute for General Microbiology, Christian-Albrechts-Universität zu Kiel, Kiel, Germany, 3 Department of Biology, Dalhousie University, Halifax, NS, Canada, 4 5 Edited by: Department of Earth Sciences, Stellenbosch University, Stellenbosch, South Africa, UMR 6539/LEMAR/IUEM, CNRS, 6 Hongbin Liu, UBO, IRD, Ifremer, Brest, France, Antarctic Climate and Ecosystems Cooperative Research Centre, Hobart, TAS, Australia, 7 The Hong Kong University of Science Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia and Technology, Hong Kong Reviewed by: Heme b is an iron-containing co-factor in hemoproteins. Heme b concentrations David Allen Hutchins, are low (<1 pmol L−1) in iron limited phytoplankton in cultures and in the field. University of Southern California, United States Here, we determined heme b in marine particulate material (>0.7 mm) from the Yonghong Bi, North Atlantic Ocean (GEOVIDE cruise – GEOTRACES section GA01), which spanned Institute of Hydrobiology (CAS), China William M. Landing, several biogeochemical regimes. We examined the relationship between heme b Florida State University, United States abundance and the microbial community composition, and its utility for mapping iron *Correspondence: limited phytoplankton. Heme b concentrations ranged from 0.16 to 5.1 pmol L−1 Evangelia Louropoulou (median = 2.0 pmol L−1, n = 62) in the surface mixed layer (SML) along the cruise track, [email protected] driven mainly by variability in biomass. However, in the Irminger Basin, the lowest heme Specialty section: b levels (SML: median = 0.53 pmol L−1, n = 12) were observed, whilst the biomass This article was submitted to was highest (particulate organic carbon, median = 14.2 mmol L−1, n = 25; chlorophyll a: Aquatic Microbiology, −1 a section of the journal median = 2.0 nmol L , n = 23) pointing to regulatory mechanisms of the heme b pool Frontiers in Microbiology for growth conservation. Dissolved iron (DFe) was not depleted (SML: median = 0.38 Received: 01 March 2019 nmol L−1, n = 11) in the Irminger Basin, but large diatoms (Rhizosolenia sp.) dominated. Accepted: 24 June 2019 Published: 11 July 2019 Hence, heme b depletion and regulation is likely to occur during bloom progression Citation: when phytoplankton class-dependent absolute iron requirements exceed the available Louropoulou E, Gledhill M, ambient concentration of DFe. Furthermore, high heme b concentrations found in the Browning TJ, Desai DK, Iceland Basin and Labrador Sea (median = 3.4 pmol L−1, n = 20), despite having similar Menzel Barraqueta J-L, Tonnard M, Sarthou G, Planquette H, Bowie AR, DFe concentrations to the Irminger Basin, were attributed to an earlier growth phase of Schmitz RA, LaRoche J and the extant phytoplankton populations. Thus, heme b provides a snapshot of the cellular Achterberg EP (2019) Regulation of the Phytoplankton Heme b Iron activity in situ and could both be used as indicator of iron limitation and contribute to Pool During the North Atlantic Spring understanding phytoplankton adaptation mechanisms to changing iron supplies. Bloom. Front. Microbiol. 10:1566. doi: 10.3389/fmicb.2019.01566 Keywords: heme b, North Atlantic, phytoplankton, diatoms, iron, limitation, GEOTRACES, GEOVIDE Frontiers in Microbiology| www.frontiersin.org 1 July 2019| Volume 10| Article 1566 fmicb-10-01566 July 11, 2019 Time: 12:11 # 2 Louropoulou et al. North Atlantic Phytoplankton Heme Regulation INTRODUCTION proxy for Fe limitation in field studies. Furthermore, fluctuations in heme b concentrations among different phytoplankton classes Iron (Fe) is an essential micro-nutrient for marine phytoplankton and species also imply that heme b abundance in the ocean could as it is associated with several key biochemical processes potentially vary according to the phytoplankton community including photosynthesis, respiration, reduction of oxidized composition (Gledhill et al., 2013, 2015; Honey et al., 2013). nitrogen species and di-nitrogen (N2) fixation (Geider and La Laboratory experiments performed on diatoms isolated Roche, 1994; Raven et al., 1999; Morel and Price, 2003). Iron from temperate and/or coastal regions (Thalassiosira weissflogii, uptake by phytoplankton occurs directly from seawater and the T. oceanica, Phaeodactylum tricornutum, and Chaetoceros availability of Fe in the surface ocean is largely controlled by rates calcitrans) and cyanobacteria (Synechococcus sp.) showed that of supply from atmospheric deposition, continental margins, decreases in the heme b cellular contents were reflected in upwelling and deep mixing entrainment of sub-surface Fe pools, decreased biomass stocks under low DFe (≤0.5 nmol L−1) relative to losses via scavenging and biological uptake (Sunda and (Honey et al., 2013; Gledhill et al., 2015). In contrast, experiments Huntsman, 1995; Geider, 1999; Tagliabue et al., 2017). Dissolved on prymnesiophytes (Emiliania huxleyi, Phaeocystis antarctica) iron (DFe) concentrations in the open ocean surface waters can and diatoms (Chaetoceros brevis), all abundant in the open be very low (<0.1 nmol L−1)(Sunda and Huntsman, 1995; Boyd ocean, showed that these species were capable of maintaining and Ellwood, 2010; Achterberg et al., 2018) and it has been well their biomass stocks (e.g., growth rates, chl a and POC) documented that low Fe availability can limit phytoplankton despite reduced intracellular heme b concentrations at low −1 growth, N2 fixation rates, and influence community structure DFe concentrations (≤0.5 nmol L )(Gledhill et al., 2015). (e.g., Greene et al., 1992; Geider and La Roche, 1994; Kolber These findings suggest that both diatoms and prymnesiophytes et al., 1994; Sunda and Huntsman, 1997; King and Barbeau, 2007; possess heme b regulation mechanisms which are expressed by Shi et al., 2007). a preferential allocation of Fe away from the hemoprotein pool In proteins, Fe is bound in Fe-sulfur clusters, Fe-oxygen-Fe in order to efficiently exploit the available Fe, reduce the overall clusters, or in Fe-porphyrin complexes also known as hemes Fe requirements and maintain growth (Gledhill et al., 2015). It (Hogle et al., 2014). Hemes function as prosthetic groups of the is likely that such a regulation mechanism reflects an overall hemoproteins (Chapman et al., 1997) and are involved in electron reduction in cellular Fe requirement until a subsistence Fe quota transfers for example during photosynthesis, respiration, nitrate is obtained, below which growth can no longer occur. reduction as well as in control, storage and transport of oxygen In the current study we determined heme b in particulate (Hogle et al., 2014). Hemes are produced in a similar manner material (>0.7 mm) sampled in the subtropical and subpolar to chlorophyll via the tetrapyrrole synthesis pathway and several North Atlantic Ocean during the GEOVIDE (GEOTRACES heme structures are present within an organism (Chapman et al., section G01) research expedition (Sarthou et al., 2018). The North 1997). The cellular heme quota is tightly coordinated, since free Atlantic Ocean is an area of high phytoplankton productivity and hemes are toxic (Espinas et al., 2012). Furthermore heme can act enhanced CO2 sequestration rates (Henson et al., 2009). Several as an Fe source for bacteria (Roe et al., 2013; Hogle et al., 2016). biogeochemical regimes exist in the North Atlantic Ocean; in Heme b (Fe protoporphyrin IX) is the most versatile heme in the temperate subtropics, nitrate limits phytoplankton growth organisms (Espinas et al., 2012) and is a constituent of the b type (Moore et al., 2008, 2013). At higher latitudes in the subpolar cytochromes, catalases, peroxidases, cytochrome p450, globin areas, during spring and summer, light is no longer a limiting and nitrate reductase (Mochizuki et al.,
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