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Marinobacter Dominates the Bacterial Community of the Ostreococcus Marinobacter Dominates the Bacterial Community of the Ostreococcus tauri Phycosphere in Culture Josselin Lupette, Raphaël Lami, Marc Krasovec, Nigel Grimsley, Hervé Moreau, Gwenaël Piganeau, Sophie Sanchez-Ferandin To cite this version: Josselin Lupette, Raphaël Lami, Marc Krasovec, Nigel Grimsley, Hervé Moreau, et al.. Marinobacter Dominates the Bacterial Community of the Ostreococcus tauri Phycosphere in Culture. Frontiers in Microbiology, Frontiers Media, 2016, 7, pp.1414. 10.3389/fmicb.2016.01414. hal-01373902 HAL Id: hal-01373902 https://hal.sorbonne-universite.fr/hal-01373902 Submitted on 27 May 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-07-01414 September 3, 2016 Time: 12:48 # 1 ORIGINAL RESEARCH published: 07 September 2016 doi: 10.3389/fmicb.2016.01414 Marinobacter Dominates the Bacterial Community of the Ostreococcus tauri Phycosphere in Culture Josselin Lupette1,2,3, Raphaël Lami4,5, Marc Krasovec1,2, Nigel Grimsley1,2, Hervé Moreau1,2, Gwenaël Piganeau1,2 and Sophie Sanchez-Ferandin1,2* 1 Sorbonne Universités, Université Pierre et Marie Curie Paris 06, UMR 7232 Biologie Intégrative des Organismes Marins, Observatoire Océanologique, Banyuls-sur-Mer, France, 2 Centre National de la Recherche Scientifique, UMR 7232 Biologie Intégrative des Organismes Marins, Observatoire Océanologique, Banyuls-sur-Mer, France, 3 CEA/CNRS/INRA/Université Grenoble Alpes, UMR 5168 Laboratoire Physiologie Cellulaire Végétale, Grenoble, France, 4 Sorbonne Universités, Université Pierre et Marie Curie Paris 06, USR 3579 Laboratoire de Biodiversité et Biotechnologies Microbiennes, Observatoire Océanologique, Banyuls-sur-Mer, France, 5 Centre National de la Recherche Scientifique, USR 3579 Laboratoire de Biodiversité et Biotechnologies Microbiennes, Observatoire Océanologique, Banyuls-sur-Mer, France Microalgal–bacterial interactions are commonly found in marine environments and are well known in diatom cultures maintained in laboratory. These interactions also exert strong effects on bacterial and algal diversity in the oceans. Small green eukaryote Edited by: algae of the class Mamiellophyceae (Chlorophyta) are ubiquitous and some species, Michael Thomas-Poulsen, University of Copenhagen, Denmark such as Ostreococcus spp., are particularly important in Mediterranean coastal lagoons, Reviewed by: and are observed as dominant species during phytoplankton blooms in open sea. Tony Gutierrez, Despite this, little is known about the diversity of bacteria that might facilitate or hinder Heriot-Watt University, Scotland Garret Suen, O. tauri growth. We show, using rDNA 16S sequences, that the bacterial community University of Wisconsin–Madison, found in O. tauri RCC4221 laboratory cultures is dominated by g-proteobacteria from USA the Marinobacter genus, regardless of the growth phase of O. tauri RCC4221, the *Correspondence: photoperiod used, or the nutrient conditions (limited in nitrogen or phosphorous) tested. Sophie Sanchez-Ferandin sophie.sanchez-ferandin@obs- Several strains of Marinobacter algicola were detected, all closely related to strains found banyuls.fr in association with taxonomically distinct organisms, particularly with dinoflagellates and coccolithophorids. These sequences were more distantly related to M. adhaerens, Specialty section: This article was submitted to M. aquaeoli and bacteria usually associated to euglenoids. This is the first time, to our Microbial Symbioses, knowledge, that distinct Marinobacter strains have been found to be associated with a a section of the journal Frontiers in Microbiology green alga in culture. Received: 25 May 2016 Keywords: Ostreococcus tauri, Marinobacter sp., picoalgae, bacteria, interactions, phytoplankton Accepted: 26 August 2016 Published: 07 September 2016 Citation: INTRODUCTION Lupette J, Lami R, Krasovec M, Grimsley N, Moreau H, Piganeau G Phytoplankton, together with viruses, bacteria, and micrograzers constitute different communities and Sanchez-Ferandin S (2016) of species which all play fundamental roles in the functioning of microbial food web (Buchan et al., Marinobacter Dominates the Bacterial 2014). Phytoplankton and bacterial communities are closely linked in coastal marine environments Community of the Ostreococcus tauri Phycosphere in Culture. (Fuhrman et al., 1980; Rooney-Varga et al., 2005; Amin et al., 2015) and bacterial–algal interactions Front. Microbiol. 7:1414. play a major role in determining bacterial and algal diversity in the ocean (Schäfer et al., 2002). doi: 10.3389/fmicb.2016.01414 Detailed knowledge of these interactions is thus crucial for understanding marine ecosystems. Frontiers in Microbiology | www.frontiersin.org 1 September 2016 | Volume 7 | Article 1414 fmicb-07-01414 September 3, 2016 Time: 12:48 # 2 Lupette et al. Microalgae–Bacteria Interactions Phytoplankton exudates can be important substrates for bacteria, problems like sensitivity to herbicides (Sanchez-Ferandin et al., especially in early phytoplankton bloom conditions (Fouilland 2013) or tolerance to polluants like arsenic (Zhang et al., 2013). et al., 2013) although other carbon sources might also be Despite the wealth of genomic data available for this species important for bacterial growth (Fouilland and Mostajir, 2010). In (Derelle et al., 2006; Blanc-Mathieu et al., 2014), the bacterial turn, some bacteria are known to inhibit or promote microalgal community associated with the O. tauri phycosphere is poorly growth (Cole, 1982; Fukami et al., 1997; de-Bashan et al., 2004). understood, and the nature of the interactions between O. tauri The volume of water closely surrounding algal cells in which and bacteria remains an open question (Abby et al., 2014). many metabolic exchanges may occur, is called the phycosphere Here, we focus on the nature and dynamics of the microbiome (Bell and Mitchell, 1972). It is analogous to the rhizosphere in of O. tauri RCC4221 across a large range of culture conditions. soils and it has direct implications for nutrient fluxes to and Surprisingly, we provide evidence that bacteria from one single from algal cells (Amin et al., 2012b). In this niche, bacteria can genus, Marinobacter (g-proteobacteria, order Alteromonadales) live freely around microalgae and interact through metabolic is largely predominant across culture conditions. fluxes via the environmental medium, or they may be more closely associated with the cells, such as epiphytic or endophytic bacteria. Epiphytic bacteria adhere to the microalgal surface (Bell MATERIALS AND METHODS and Mitchell, 1972; Shapiro et al., 1998) with a tight functional association (Middelboe et al., 1995; Smith et al., 1995; Grossart Ostreococcus tauri RCC4221 Culture in et al., 2005). Endophytic bacteria are able to develop inside Different Conditions microalgal cells and have been seen in Chlorophyta (Kawafune Ostreococcus tauri strain RCC4221 was isolated in 1994 et al., 2012). Both commensalism and/or competition for from the North-West Mediterranean Thau lagoon (Courties micronutrients may occur between phytoplankton and bacteria et al., 1994) and maintained in the laboratory (cultures and (Bratbak and Thingstad, 1985; Amin et al., 2012a). Bacteria might cryopreservation). The O. tauri strain was grown in liquid positively (stimulation) or negatively (inhibition, alteration medium in aerated flasks (Sarstedt), in growth chambers at of physiology, death) influence phytoplankton dynamics. As 20±1◦C and white light at around 100 mmol photons.m−2.sec−1 examples, stimulation of phytoplankton growth by bacteria can using three photoperiods (LD 08:16; LD 12:12; and LD 14:10). occur via the production of vitamins (Haines and Guillard, 1974; Two culture media were prepared, one with natural sea water, Kurata, 1986; Croft et al., 2005; Kuo and Lin, 2013), siderophores L1-MOLA (Guillard and Hargraves, 1993) and one with artificial (Martinez et al., 2000, 2003; Amin et al., 2009) or phytohormones sea water, F/2-ESAW (Harrison et al., 1980). Both L1-MOLA (de-Bashan et al., 2008) like auxin (Gonzalez and Bashan, 2000). and F/2-ESAW were produced by adding nitrogen (NaNO3), In contrast, bacteria can even kill the algae by the secretion of phosphorus (NaH2PO4) and vitamins (B1, B12, and H) but algicidal compounds (Mayali and Azam, 2004). at different concentrations (Supplementary Table S1). Only Some studies demonstrated the presence of specific L1-MOLA was prepared from seawater, collected from 20 m bacterial communities associated with algal blooms in marine below sea level at the MOLA station and kept several weeks environments (Gonzalez et al., 2000; Buchan et al., 2014). in the dark before use. The seawater was filtered through In axenic (i.e., exempt of bacteria) microalgal monocultures, 0.22 mm and autoclaved. For nutrient limitation experiments, microalgal growth may be unstable and prone to perturbation four conditions were tested: L1-MOLA, F/2-ESAW, F/2-ESAW (Kazamia et al., 2014), highlighting again the importance 50%N (half nitrogen concentration), and F/2-ESAW 10%P (one of microalgalbacterial interactions, not only
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