Abstract

Interactions between phytoplankton and bacteria play a central role in mediating biogeochemical cycling and food web structure in the ocean. However, deciphering the chemical drivers of these interspecies interactions remains challenging. Here, we report the isolation of 2-heptyl-4-quinolone (HHQ), released by Pseudoalteromonas piscicida, a marine gamma-proteobacteria previously reported to induce phytoplankton mortality through a hitherto unknown algicidal mechanism. HHQ functions as both an antibiotic and a bacterial signaling molecule in cell–cell communication in clinical infection models. Co-culture of the bloom-forming coccolithophore, Emiliania huxleyi with both live P. piscicida and cell-free filtrates caused a significant decrease in algal growth. Investigations of the P. piscicida exometabolome revealed HHQ, at nanomolar concentrations, induced mortality in three strains of E. huxleyi. Mortality of E. huxleyi in response to HHQ occurred slowly, implying static growth rather than a singular loss event (e.g., rapid cell lysis). In contrast, the marine chlorophyte, Dunaliella tertiolecta and diatom, Phaeodactylum tricornutum were unaffected by HHQ exposures. These results suggest that HHQ mediates the type of inter-domain interactions that cause shifts in phytoplankton population dynamics. These chemically mediated interactions, and other like it, ultimately influence large-scale oceanographic processes.

Highlights

  • In the marine environment, interactions between bacteria and eukaryotic phytoplankton are pervasive and drive oceanic biogeochemical cycles (Legendre and Rassoulzadegan, 1995), and can have consequences for both microbial communities (Bratbak and Thingstad, 1985) and structuring of marine food webs (Azam et al, 1983)

  • We found that the presence of P. piscicida resulted in mortality of E. huxleyi, and used bioassay-guided fractionation to identify the responsible chemical mediator(s) of this interaction

  • Exposure to crude extracts resulted in significant mortality for E. huxleyi (Figure 1B; p < 0.001), with negative growth rates for E. huxleyi when exposed to either concentration of crude extract

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Summary

Introduction

Interactions between bacteria and eukaryotic phytoplankton are pervasive and drive oceanic biogeochemical cycles (Legendre and Rassoulzadegan, 1995), and can have consequences for both microbial communities (Bratbak and Thingstad, 1985) and structuring of marine food webs (Azam et al, 1983). Bacteria–phytoplankton interactions are complex, being both temporally variable (Danger et al, 2007) and species-specific (Fukami et al, 1997), and remain largely enigmatic. These interactions can be beneficiary, as bacteria and phytoplankton can support the growth of one another via the exchange or recycling. The intricate relationships between these two kingdoms are often mediated via excreted compounds that can direct communication between the two organisms Identifying these released compounds, and their influence on the population dynamics of both phytoplankton and bacteria, will enhance our understanding of the role of “infochemicals” on large-scale biogeochemical processes. Pseudoalteromonas species have been implicated in producing algal-lytic compounds that cause mortality in dinoflagellates (Skerratt et al, 2002; Kim et al, 2009), diatoms (Mitsutani et al, 2001), and raphidophytes (Lovejoy et al, 1998); in each of these cases the causative chemical compound is yet unidentified

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