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A Bacterial Quorum-Sensing Precursor Induces Mortality in the Marine Coccolithophore, Emiliania Huxleyi

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A Bacterial Quorum-Sensing Precursor Induces Mortality in the Marine Coccolithophore, Emiliania Huxleyi Haverford College Haverford Scholarship Faculty Publications Biology 2016 A Bacterial Quorum-Sensing Precursor Induces Mortality in the Marine Coccolithophore, Emiliania huxleyi E. L. Harvey R. W. Deering D. C. Rowley Kristen E. Whalen Haverford College, [email protected] Follow this and additional works at: https://scholarship.haverford.edu/biology_facpubs Repository Citation Harvey et al. "A Bacterial Quorum-Sensing Precursor Induces Mortality in the Marine Coccolithophore, Emiliania huxleyi."Frontiers in Microbiology, 7(59):1-12, (2016). This Journal Article is brought to you for free and open access by the Biology at Haverford Scholarship. It has been accepted for inclusion in Faculty Publications by an authorized administrator of Haverford Scholarship. For more information, please contact [email protected]. ORIGINAL RESEARCH published: 03 February 2016 doi: 10.3389/fmicb.2016.00059 A Bacterial Quorum-Sensing Precursor Induces Mortality in the Marine Coccolithophore, Emiliania huxleyi Elizabeth L. Harvey1*†, Robert W. Deering2, David C. Rowley2,AbrahimElGamal3, Michelle Schorn3, Bradley S. Moore3, Matthew D. Johnson4, Tracy J. Mincer5 and Kristen E. Whalen5*† 1 Department of Marine Sciences, Skidaway Institute of Oceanography, University of Georgia, Savannah, GA, USA, 2 Department of Biomedical and Pharmaceutical Sciences, University of Rhode Island, Kingston, RI, USA, 3 Scripps Institution of Oceanography, University of California at San Diego, La Jolla, CA, USA, 4 Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA, 5 Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA Interactions between phytoplankton and bacteria play a central role in mediating Edited by: biogeochemical cycling and food web structure in the ocean. However, deciphering Xavier Mayali, the chemical drivers of these interspecies interactions remains challenging. Here, we Lawrence Livermore National Laboratory, USA report the isolation of 2-heptyl-4-quinolone (HHQ), released by Pseudoalteromonas Reviewed by: piscicida, a marine gamma-proteobacteria previously reported to induce phytoplankton Assaf Vardi, mortality through a hitherto unknown algicidal mechanism. HHQ functions as both Weizmann Institute of Science, Israel an antibiotic and a bacterial signaling molecule in cell–cell communication in clinical Travis Blake Meador, University of Bremen, Germany infection models. Co-culture of the bloom-forming coccolithophore, Emiliania huxleyi *Correspondence: with both live P. piscicida and cell-free filtrates caused a significant decrease in algal Elizabeth L. Harvey growth. Investigations of the P. piscicida exometabolome revealed HHQ, at nanomolar [email protected]; Kristen E. Whalen concentrations, induced mortality in three strains of E. huxleyi. Mortality of E. huxleyi [email protected] in response to HHQ occurred slowly, implying static growth rather than a singular loss †These authors have contributed event (e.g., rapid cell lysis). In contrast, the marine chlorophyte, Dunaliella tertiolecta and equally to this work. diatom, Phaeodactylum tricornutum were unaffected by HHQ exposures. These results Specialty section: suggest that HHQ mediates the type of inter-domain interactions that cause shifts in This article was submitted to phytoplankton population dynamics. These chemically mediated interactions, and other Aquatic Microbiology, a section of the journal like it, ultimately influence large-scale oceanographic processes. Frontiers in Microbiology Keywords: infochemicals, algicidal compound, bacteria–phytoplankton interaction, HHQ, Pseudoalteromonas, Received: 23 October 2015 Emiliania huxleyi, IC50, mortality Accepted: 13 January 2016 Published: 03 February 2016 Citation: INTRODUCTION Harvey EL, Deering RW, Rowley DC, El Gamal A, Schorn M, Moore BS, In the marine environment, interactions between bacteria and eukaryotic phytoplankton are Johnson MD, Mincer TJ pervasive and drive oceanic biogeochemical cycles (Legendre and Rassoulzadegan, 1995), and and Whalen KE (2016) A Bacterial can have consequences for both microbial communities (Bratbak and Thingstad, 1985)and Quorum-Sensing Precursor Induces structuring of marine food webs (Azam et al., 1983). Bacteria–phytoplankton interactions are Mortality in the Marine Coccolithophore, Emiliania huxleyi. complex, being both temporally variable (Danger et al., 2007) and species-specific (Fukami Front. Microbiol. 7:59. et al., 1997), and remain largely enigmatic. These interactions can be beneficiary, as bacteria doi: 10.3389/fmicb.2016.00059 and phytoplankton can support the growth of one another via the exchange or recycling Frontiers in Microbiology | www.frontiersin.org 1 February 2016 | Volume 7 | Article 59 Harvey et al. Bacterial Infochemical Induces Phytoplankton Mortality of nutrients (Azam et al., 1983); however, the interaction can MATERIALS AND METHODS also be detrimental, resulting in phytoplankton morbidity or mortality (Mayali and Azam, 2004). The intricate relationships Culture Conditions and Crude Extract between these two kingdoms are often mediated via excreted compounds that can direct communication between the two Preparation organisms. Identifying these released compounds, and their A pure culture of P. piscicida was isolated from open ocean plastic influence on the population dynamics of both phytoplankton debris in the North Atlantic (Mincer culture ID; A757; Whalen et al., 2015), cryopreserved in 10% sterile DMSO, and stored at and bacteria, will enhance our understanding of the role of ◦ “infochemicals” on large-scale biogeochemical processes. −85 C prior to experiments. From these stocks, multiple ‘starter’ The marine genus Pseudoalteromonas constitutes 0.5–6.0% cultures were prepared by inoculating 8 mL of TSW media (1 g tryptone in 1 L of 75:25 seawater/MilliQ water) with 100 μLof of bacterial species globally (Wietz et al., 2010), and has ◦ been found in seawater, marine sediments, and associated cryopreserved culture, and then incubated at 23 Cwhileshaking with marine eukaryotes (Bowman, 2007; Skovhus et al., 2007; at 100 rpm for 3 days. After 3 days, 2 mL of ‘starter’ culture was Sneed et al., 2014). Secondary metabolites secreted by members used to inoculate seven, 1.5 L Fernbach flasks of TSY media (1 g tryptone, 1 g yeast extract, 75% seawater), the newly inoculated of this genus fulfill a variety of ecological roles, including ◦ involvement in chemical protection, settlement, induction of cultures were then grown at 100 rpm for 8 days at 23 C. On day metamorphosis in marine invertebrates, and commercially, as 7, 20 mL (approximately weight = 7.8g)of1:1mixtureofsterile antifouling, antifungal agents (Bowman, 2007; Ross et al., 2014; Amberlite R XAD-7 and XAD-16 resin that had been extensively Sneed et al., 2014). Moreover, Pseudoalteromonas species have washed in organic solvent, dried, and autoclaved was added to been implicated in producing algal-lytic compounds that cause each 1.5 L culture. Twenty-four hours later (day 8), the resin was mortality in dinoflagellates (Skerratt et al., 2002; Kim et al., 2009), filtered from the bacterial culture through combusted stainless diatoms (Mitsutani et al., 2001), and raphidophytes (Lovejoy steel mesh under gentle vacuum (<5inHg),desaltedbyrinsing et al., 1998); however, in each of these cases the causative chemical with MilliQ water, pooled, and allowed to dry overnight at room compound is yet unidentified. temperature. Bacterial metabolites were eluted from the resin first In order to gain a more mechanistic understanding of in 800 mL of (1:1) methanol (MeOH):dichloromethane (DCM), followed by 800 mL of methanol. This crude extract was dried this chemically mediated phytoplankton mortality, we exposed ◦ the globally important coccolithophore, Emiliania huxleyi to under vacuum centrifugation and stored at −85 C until testing cultures of Pseudoalteromonas piscicida. E. huxleyi plays a in phytoplankton growth assays. predominant role in oceanic carbon (Balch et al., 1992; Iglesias- Emiliania huxleyi (Plymouth Algal Culture Collection: Rodriguez et al., 2008)andsulfur(Simo, 2001) cycling; therefore, DHB624 and National Center for Marine Algae: CCMP374, understanding the factors that mediate the population abundance CCMP379), Dunaliella tertiolecta (CCMP1320), and and distribution of this algal species is important for predicting Phaeodactylum tricornutum (CCMP2561) were used in its role in marine nutrient cycling and global climate. Further, these experiments. All phytoplankton cultures were grown E. huxleyi has been shown to form complex relationships in 0.2 μm sterile-filtered, autoclavedseawater(FSW),enriched with bacteria. For example, it has been observed that the with f/2 (P. tricornutum) or f/2 -Si (all other species) media Roseobacter, Phaeobacter gallaeciensis maintains a mutualistic- (Guillard, 1975). All cultures were maintained on a 12:12 h turned-to-parasitic relationship with E. huxleyi dependent on the light:dark at 18◦C, salinity of approximately 20 psu, and light − − metabolic stage of the algae (Seyedsayamdost et al., 2011). While intensity of 85–100 μmol photon m 2 s 1. Hereafter, these no direct relationship between a Pseudoalteromonas species conditions will be referred to as general culturing conditions. and E. huxleyi has been established, Seymour et al. (2010) Phytoplankton cultures were transferred every 7–10 days to found that Pseudoalteromonas haloplanktis exhibited strong maintain exponential growth. Unless specified,
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