Adsorptive exchange of biominerals facilitates viral infection

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Adsorptive exchange of biominerals facilitates viral infection

A defining characteristic of marine coccolithophores is the ability to produce nanopatterned calcite biominerals (coccoliths), which profoundly impact the marine carbon cycle. These coccoliths, which are produced intracellularly and extruded through the cell membrane upon maturation, are incorporated into a surrounding coccosphere and serve to ballast photosynthetically-fixed carbon to ocean depths. Calcification is a highly dynamic process. Discarded, ‘free’ coccoliths routinely slough off into the external milieu, outnumbering cells in the environment by orders of magnitude and revealing mesoscale oceanic blooms to Earth-observing satellites through their highly refractive nature. These free-floating, adsorptive, dense coccoliths are frequently incorporated into marine particles to facilitate carbon export.

Fig. 1. Xenospheres of coccolithophores are globally distributed across diverse oceanic regions.SEM images of xenospheres composed of: (A) Two different Emiliania huxleyi coccolith morphotypes in the Northeast Atlantic (North Atlantic Virus Infection of Coccolithophores Expedition (NA-VICE;http://www.bco-dmo.org/project/2136); (B) Two different E. huxleyi coccolith morphotypes and a coccolith from another coccolithophore species (possibly Gephyrocapsa oceanica) observed in the Mediterranean Sea [courtesy of Dr. Barbara D’Amario (18)]; (C) E. huxleyi coccoliths and a coccolith from Syracosphaera corolla observed in English Channel [courtesy of Dr. Alison Taylor]; (D) E. huxleyi coccoliths and coccoliths from Rhabdosphaera clavigera observed in the North Aegean Sea [courtesy of Dr. Margarita Dimiza and Odysseas Archontikis (30)]; (E, F) E. huxleyi coccoliths and coccoliths from Gephyrocapsa collected from Uranouchi Bay, Kochi Prefecture, Japan [courtesy of the Electronic Microfossil Image Data Base System (EMIDAS; http://www.emidas.org/) and Dr. Kyoko Hagino (31)]; (G) E. huxleyi coccoliths and a coccolith from G. oceanica in the Gulf of Aquaba (21); (H) Two different E. huxleyi coccolith morphotypes collected during the 4th Indian Southern Ocean Expedition (23); (I) Two different E. huxleyi coccolith morphotypes and (J) E. huxleyi coccoliths and a coccolith from Discosphaeratubiera, both observed in the Santa Barbara Channel [images from Dr. Paul Matson]. (K) Relative distribution of xenospheres (blue) compared to E. huxleyi (grey), G. oceanica (light grey), and other coccolithophore species (black) with uniform, homogenous coccospheres (n=1178). Images from both (I) and (J), as well as data in (K) derive from surface populations across all stations of the 2014 Plumes and Blooms cruise (http://www.oceancolor.ucsb.edu/plumes_and_blooms/). (A-J) Color shading for all SEM images designates E. huxleyi Type A morphotype (blue), other E. huxleyi morphotypes (Type O and Type Overcalcified A; purple), and coccoliths from other coccolithophore species (orange). Scale bars are provided for size reference.

The interactive ecosystem role(s) of free coccolith biominerals have remained unexplored. To date, they have been thought off as passive, inconsequential, planktonic minerals. Using extensive environmental observations, lab-based experiments, and theoretical modeling, we highlight novel interactive and consequential roles of coccolith exchange that hinge on their adsorptive capabilities. We show that free coccoliths are highly adsorptive biominerals that readily interact with cells to form chimeric coccospheres [and/or xenospheres, which have been observed across the global ocean (Fig. 1)] and with viruses to facilitate infection, which can terminate blooms (Fig. 2). Adsorption is mediated by organic matter associated with the coccolith base plate and varies with biomineral morphology. Furthermore, the very high encounter rates of coccoliths with both viruses and cells make them effective catalysts of infection that can circumvent chronically low encounter rates between cells and viruses alone. Our findings argue that coccolith exchange is widespread and a novel, unexplored layer in the ecophysiology of calcification.

Fig. 2. The multifaceted roles of coccoliths in E. huxleyi-EhV interactions. A conceptual model highlighting the mulitfaceted roles of coccoliths during viral infection. The top section (panels i-iii; shaded blue) represents the beneficial roles of coccoliths to host cells by delaying infection as described in a previous study (5); the bottom section (panels iv-vi; shaded pink) highlights of the antagonistic roles of coccoliths to host cells by facilitating infection via viroliths as described in this study. (i) Coccoliths can help delay infection by preventing viruses from contacting the cell surface; (ii) exposure to viruses induces the production of a host-derived, unidentifed infochemical (yellow) that triggers coccolith shedding; (iii) coccolith shedding occurs prior to cell lysis, increasing the concentration of naked cells and free coccoliths within a population, with the coccoliths adsorbing and removing free viruses from the surrounding milleu; (iv) virus adsorption to free coccoliths leads to the formation of viroliths; (v) virolith adsorption to cells increases the encounter rate of viruses to cells and promotes delivery of infectious EhVs to the cell surface; (vi) viral production and lysis of host cells, in conjuction with virus-induced cocolith shedding, increases the likelihood of further virolith formation.

The dynamic exchange of coccolith biominerals has profound ecological and biogeochemical implications. It puts these biominerals at the heart of interactive arms races between coccolithophore hosts and viruses that toggle cells between life and death. Coccoliths can act as physical protection against viruses but also as a catalyst for death, adsorbing and delivering viruses to the cell for successful infection, analogous to a virulent ‘Trojan Horse’. Persistent coccolith adsorption and exchange fundamentally deviates from prominent paradigms in our field. It has been assumed that coccospheres were produced entirely from within by actively calcifying cells. We show that coccospheres can be made solely of adsorbed coccoliths. Furthermore, demonstration of successful viral infection through biomineral hitchhiking increases host-virus encounters by nearly an order of magnitude (compared to free-floating viruses), critically catalyzing infection and fundamentally altering how we view biomineral-cell-virus interactions in the environment.