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Light-independent mechanisms of virion inactivation in coastal marine systems

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Abstract

The hypothesis that specific components of seawater, such as particulate, dissolved and colloidal organic and inorganic material, render virions non-infective has long been postulated, but never rigorously tested. To address this hypothesis, the plaque assay method was used to derive infective decay rates, k, of two bacteriophages—P1 (marine host: PWH3a) and T4 (enteric host: E. coli B). We compared k values of bacteriophage suspended in serial filtrations of seawater, with and without autoclaving and UV oxidation. Both phages exhibited reduced decay rates in particle-free water (<0.2 μm) compared to <10 μm filtrate. The largest decrease in virion decay rates was achieved by autoclaving the 0.2 μm filtrate. UV oxidation of <0.2 μm filtrate, however, yielded higher decay rates than observed in autoclaved treatments. The lowest k values were seen in ultra-filtered seawater (<10 kDa). Exposure to a wide range of concentrations of Pronase E (a proteolytic enzyme), inorganic clay (kaolinite or montmorillonite), and organic particles (phytoplankton debris) did not promote phage inactivation. P1 infective titers were also not consistently reduced by exposures to axenic cultures of a resistant host mutant (PWH3a-R) and a non-host marine bacterium (MB-5). Finally, phage were exposed to a range of temperatures to derive activation energies required for phage inactivation. Application of the Arrhenius model to inactivation of T4 and P1 yielded activation energies (E a) of 49 and 40 kJ mol−1, respectively. This is the first comprehensive analysis in which specific seawater components were assayed for their ability to inactivate bacteriophage. Inactivation of these phage does not appear to depend on capsomere denaturation, proteolytic extracellular enzymes, sorption to non-host bacteria, clay particles or particulate organic debris, but is accelerated by naturally occurring particles, which include living organisms, and heat-labile colloids and macromolecules >10 kDa.

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Acknowledgments

The authors are indebted to D. O’Shaunessy and J. Otto for their outstanding technical assistance and Drs. S. Munch, C. Gobler, and J. Collier for their expert advice. We would also like to thank Dr. H. G. Dam and Dr. D. E. Avery, as well as the editor and two anonymous reviewers for their insightful comments regarding this manuscript. A portion of this research fulfilled requirements for completion of M. Finiguerra’s Masters of Science degree. This research was funded by the U.S. National Oceanic and Atmospheric Administration’s Oceans and Human Health Initiative, grant #NA-04OAR4600197. School of Marine and Atmospheric Sciences contribution # 1400.

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Authors and Affiliations

  1. School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, 11794, USA

    Michael B. Finiguerra, Douglas F. Escribano & Gordon T. Taylor

  2. Department of Marine Sciences, University of Connecticut, Groton, 1080 Shennecossett Road, Groton, CT, 06340, USA

    Michael B. Finiguerra

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  1. Michael B. Finiguerra
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  2. Douglas F. Escribano
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Correspondence to Michael B. Finiguerra.

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Handling editor: Pierluigi Viaroli

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Finiguerra, M.B., Escribano, D.F. & Taylor, G.T. Light-independent mechanisms of virion inactivation in coastal marine systems. Hydrobiologia 665, 51–66 (2011). https://doi.org/10.1007/s10750-011-0603-x

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