Phage ecology

Bacteriophages (phages), potentially the most numerous "organisms" on Earth, are the viruses of bacteria (more generally, of prokaryotes^[1]). Phage ecology is the study of the interaction of bacteriophages with their environments.^[2]

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Introduction to phage ecology

Vastness of phage ecology

Phages are obligate intracellular parasites meaning that they are able to reproduce only while infecting bacteria. Phages therefore are found only within environments that contain bacteria. Most environments contain bacteria, including our own bodies (there called normal flora). Often these bacteria are found in large numbers. As a consequence, phages are found almost everywhere.

As a rule of thumb, many phage biologists expect that phage population densities will exceed bacterial densities by a ratio of 10-to-1 or more (VBR or virus-to-bacterium ratio; see [1] for a summary of actual data). As there exist estimates of bacterial numbers on Earth of approximately 10³⁰[2], there consequently is an expectation that 10³¹ or more individual virus (mostly phage[3]) particles exist[4], making phages the most numerous category of "organisms" on our planet.

Bacteria (along with archaeabacteria) appear to be highly diverse and there possibly are millions of species[5]. Phage-ecological interactions therefore are quantitatively vast: huge numbers of interactions. Phage-ecological interactions are also qualitatively diverse: There are huge numbers of environment types, bacterial-host types[6], and also individual phage types[7]).

Studying phage ecology

The scale of phage ecology is at once both exhilarating and intimidating. As a guiding principle toward understanding phage ecology we therefore seek generalizations, plus look to more established scientific disciplines for guidance, the most obvious being general ecology. Toward that end we can speak of phage "organismal" ecology, population ecology, community ecology, and ecosystem ecology. Phage ecology from these perspectives will be described in turn (re: links in previous sentence).

Phage ecology also may be considered (though mostly less well formally explored) from perspectives of phage behavioral ecology, evolutionary ecology, functional ecology, landscape ecology, mathematical ecology, molecular ecology, physiological ecology (or ecophysiology), and spatial ecology. Phage ecology additionally draws (extensively) from microbiology, particularly in terms of environmental microbiology, but also from an enormous catalog (90 years) of study of phage and phage-bacterial interactions in terms of their physiology and, especially, their molecular biology.

• Suggestions for further reading are provided below.

Phage "organismal" ecology

Phage "organismal" ecology is primarily the study of the evolutionary ecological impact of phage growth parameters:

• latent period, plus
  • eclipse period (or simply "eclipse")
  • rise period (or simply "rise")
• burst size, plus
  • rate of intracellular phage-progeny maturation
• adsorption constant, plus
  • rates of virion diffusion
  • virion decay (inactivation) rates
• host range, plus
  • resistance to restriction
  • resistance to abortive infection
• various temperate-phage properties, including
  • rates of reduction to lysogeny
  • rates of lysogen induction
• the tendency of at least some phage to enter into (and then subsequently leave) a not very well understood state known (inconsistently) as pseudolysogeny^[3]

Another way of envisioning phage "organismal" ecology is that it is the study of phage adaptations that contribute to phage survival and transmission to new hosts or environments. Phage "organismal" ecology is the most closely aligned of phage ecology disciplines with the classical molecular and molecular genetic analyses of bacteriophage.

From the perspective of ecological subdisciplines, we can also consider phage behavioral ecology, functional ecology, and physiological ecology under the heading of phage "organismal" ecology. However, as noted, these subdisciplines are not as well developed as more general considerations of phage "organismal" ecology. Phage growth parameters often evolve over the course of phage experimental adaptation studies.

• Suggestions for further reading are provided below.

Historical overview

In the mid 1910s, when phage were first discovered, the concept of phage was very much a whole-culture phenomenon (like much of microbiology^[4]), where various types of bacterial cultures (on solid media, in broth) were visibly cleared by phage action. Though from the start there was some sense, especially by Fėlix d'Hėrelle, that phage consisted of individual "organisms", in fact it wasn't until the late 1930s through the 1940s that phage were studied, with rigor, as individuals, e.g., by electron microscopy and single-step growth experiments (example of latter). Note, though, that for practical reasons much of "organismal" phage study is of their properties in bulk culture (many phage) rather than the properties of individual phage virions or individual infections.

This somewhat whole-organismal view of phage biology saw its heyday during the 1940s and 1950s, before giving way to much more biochemical, molecular genetic, and molecular biological analyses of phage, as seen during the 1960s and onward. This shift, paralleled in much of the rest of microbiology[8], represented a retreat from a much more ecological view of phages (first as bacterial killers, and then as organisms unto themselves). However, the organismal view of phage biology lives on as a foundation of phage ecological understanding. Indeed, it represents a key thread that ties together the ecological thinking on phage ecology with the more "modern" considerations of phage as molecular model systems.

Methods

The basic experimental toolkit of phage "organismal" ecology consists of the single-step growth (or one-step growth; example) experiment and the phage adsorption curve (example). Single-step growth is a means of determining the phage latent period (example), which is approximately equivalent (depending on how it is defined) to the phage period of infection. Single-step growth experiments also are employed to determine a phage's burst size, which is the number of phage (on average) that are produced per phage-infected bacterium.

The adsorption curve is obtained by measuring the rate at which phage virion particles (see [9]) attach to bacteria. This is usually done by separating free phage from phage-infected bacteria in some manner so that either the loss of not currently infecting (free) phage or the gain of infected bacteria may be measured over time.

• Suggestions for further reading are provided below.

Phage population ecology

A population is a group of individuals which either do or can interbreed or, if incapable of interbreeding, then are recently derived from a single individual (a clonal population). Population ecology considers characteristics that are apparent in populations of individuals but either are not apparent or are much less apparent among individuals. These characteristics include so-called intraspecific interactions, that is between individuals making up the same population, and can include competition as well as cooperation. Competition can be either in terms of rates of population growth (as seen especially at lower population densities in resource-rich environments) or in terms of retention of population sizes (seen especially at higher population densities where individuals are directly competing over limited resources). Respectively, these are population-density independent and dependent effects.

Phage population ecology considers issues of rates of phage population growth, but also phage-phage interactions as can occur when two or more phage adsorb an individual bacterium.

• Suggestions for further reading are provided below.

Phage community ecology

A community consists of all of the biological individuals found within a given environment (more formally, within an ecosystem), particularly when more than one species is present. Community ecology studies those characteristics of communities that either are not apparent or which are much less apparent if a community consists of only a single population. Community ecology thus deals with interspecific interactions. Interspecific interactions, like intraspecific interactions, can range from cooperative to competitive but also to quite antagonistic (as are seen, for example, with predator-prey interactions). An important consequence of these interactions is coevolution.

The interaction of phage with bacteria is the primary concern of phage community ecologists. Phage, however, are capable of interacting with species other than bacteria, e.g., such as phage-encoded exotoxin interaction with animals[10]. Phage therapy is an example of applied phage community ecology.

• Suggestions for further reading are provided below.

Phage ecosystem ecology

An ecosystem consists of both the biotic and abiotic components of an environment. Abiotic entities are not alive and so an ecosystem essentially is a community combined with the non-living environment within which that ecosystem exists. Ecosystem ecology naturally differs from community ecology in terms of the impact of the community on these abiotic entities, and vice versa. In practice, the portion of the abiotic environment of most concern to ecosystem ecologists is inorganic nutrients and energy.

Phage impact the movement of nutrients and energy within ecosystems primarily by lysing bacteria. Phage can also impact abiotic factors via the encoding of exotoxins (a subset of which are capable of solubilizing the biological tissues of living animals[11]). Phage ecosystem ecologists are primarily concerned with the phage impact on the global carbon cycle, especially within the context of a phenomenon know as the microbial loop.

An interactive and highly simplified model for an evolving ecology of phages and bacteria can be found on Cmol.

• Suggestions for further reading are provided below.

Further reading

Provided are suggested readings gleaned mostly from the secondary literature, presented by category. When available, links are being provided to full text, online versions of articles, or to abstracts if full text versions are not available. Avoided are linking directly to PDFs or to materials posted on personal web sites, unless the latter is where an article was "published". An approximation of ASM (American Society for Microbiology) conventions are used throughout. Some articles may be found online on personal web pages^[5]. An extensive list of phage monographs also exists, though these do not by and large have a strong phage ecology emphasis.

General Reviews

These are articles that provide a good overview of general aspects phage ecology.

• Weinbauer, M.G., Agis, M., Bonilla-Findji, O., Malits, A., and C. Winter 2007. Bacteriophage in the Environment, p. 61-92. In S. Mc grath and D. van Sinderen (eds.), Bacteriophage: Genetics and Molecular Biology. Caister Academic Press, Norfolk, UK. ISBN 978-1-904455-14-1, Google Books
• Abedon, S. T. 2006. Phage ecology, p. 37-46. In R. Calendar and S. T. Abedon (eds.), The Bacteriophages. Oxford University Press, Oxford. ISBN 0-19-514850-9, Google Books
• Breitbart, M., F. Rohwer, and S. T. Abedon. 2005. Phage ecology and bacterial pathogenesis, p. 66-91. In M. K. Waldor, D. I. Friedman, and S. L. Adhya (eds.), Phages: Their Role in Bacterial Pathogenesis and Biotechnology. ASM Press, Washington DC. ISBN 1-55581-307-0, Google Books
• Brüssow, H., and E. Kutter. 2005. Phage ecology, p. 129-164. In E. Kutter and A. Sulakvelidze (eds.), Bacteriophages: Biology and Application. CRC Press, Boca Raton, Florida. ISBN 0-8493-1336-8, Google Books
• Chibani-Chennoufi, S., A. Bruttin, M. L. Dillmann, and H. Brüssow. 2004. Phage-host interaction: an ecological perspective. J. Bacteriol. 186:3677-3686. full text
• Weinbauer, M. G. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28:127-181. abstract
• Paul, J. H., and C. A. Kellogg. 2000. Ecology of bacteriophages in nature, p. 211-246. In C. J. Hurst (ed.), Viral Ecology. Academic Press, San Diego. ISBN 0-12-362675-7
• Levin, B. R., and Richard Lenski. 1985. Bacteria and phage: A model system for the study of the ecology and co-evolution of hosts and parasites, p. 227-242. In D. Rollinson and R. M. Anderson (eds.), Ecology and Genetics of Host-Parasite Interactions. Academic Press, London. ISBN 0-12-593690-7
• Anderson, E. S. 1957. The relations of bacteriophages to bacterial ecology, p. 189-217. In R. E. O. Williams and C. C. Spicer (eds.), Microbial Ecology. Cambridge University Press, London.

Books

A handful of books provide good (if in many cases dated) overviews of various aspects of phage ecology.

• Abedon, S. T. (March, 2008-anticipated publication date). Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, UK.
• Mc Grath, S. and van Sinderen, D. 2007. Bacteriophage: Genetics and Molecular Biology. Caister Academic Press, UK. ISBN 978-1-904455-14-1, Google Books
• Ackermann, H.-W., and M. S. DuBow. 1987. Viruses of Prokaryotes, Volume 1, General Properties of Bacteriophages. CRC Press, Boca Raton, Florida. ISBN 0-8493-6056-0
• Ackermann, H.-W., and M. S. DuBow. 1987. Viruses of Prokaryotes, Volume 2, Natural Groups of Bacteriophages. CRC Press, Boca Raton, Florida. ISBN 0-8493-6056-0
• Goyal, S. M., C. P. Gerba, and G. Bitton. 1987. Phage Ecology. CRC Press, Boca Raton, Florida. ISBN 0-471-82419-4

Phage "organismal" ecology (suggested reading)

None of these reviews are devoted exclusively to issues of phage "organismal" ecology, but of those reviews of phage ecology, these cover that subject most extensively. See virulence evolution, etc., on the phage experimental evolution page for additional references. Return to phage "organismal" ecology.

• Abedon, S. T. 2006. Phage ecology, p. 37-46. In R. Calendar and S. T. Abedon (eds.), The Bacteriophages. Oxford University Press, Oxford. ISBN 0-19-514850-9, Google Books
• Breitbart, M., F. Rohwer, and S. T. Abedon. 2005. Phage ecology and bacterial pathogenesis, p. 66-91. In M. K. Waldor, D. I. Friedman, and S. L. Adhya (eds.), Phages: Their Role in Bacterial Pathogenesis and Biotechnology. ASM Press, Washington DC. ISBN 1-55581-307-0, Google Books
• Brüssow, H., and E. Kutter. 2005. Phage ecology, p. 129-164. In E. Kutter and A. Sulakvelidze (eds.), Bacteriophages: Biology and Application. CRC Press, Boca Raton, Florida. ISBN 0-8493-1336-8, Google Books
• Chibani-Chennoufi, S., A. Bruttin, M. L. Dillmann, and H. Brüssow. 2004. Phage-host interaction: an ecological perspective. J. Bacteriol. 186:3677-3686. full text
• Weinbauer, M. G. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28:127-181. abstract
• Paul, J. H., and C. A. Kellogg. 2000. Ecology of bacteriophages in nature, p. 211-246. In C. J. Hurst (ed.), Viral Ecology. Academic Press, San Diego. ISBN 0-12-362675-7
• Robb, F. T., and R. T. Hill. 2000. Bacterial viruses and hosts: Influence of culturable state, p. 199-208. In R. R. Colwell and D. J. Grimes (eds.), Nonculturable Microorganisms in the Environment. ASM Press, Washington, D.C. ISBN 1-55581-196-5
• Schrader, H. S., J. O. Schrader, J. J. Walker, N. B. Bruggeman, J. M. Vanderloop, J. J. Shaffer, and T. A. Kokjohn. 1997. Effects of host starvation on bacteriophage dynamics, p. 368-385. In R. Y. Morita (ed.), Bacteria in Oligotrophic Environments. Starvation-Survival Lifestyle. Chapman & Hall, New York. ISBN 0-412-10661-2
• Kutter, E., E. Kellenberger, K. Carlson, S. Eddy, J. Neitzel, L. Messinger, J. North, and B. Guttman. 1994. Effects of bacterial growth conditions and physiology on T4 infection, p. 406-418. In J. D. Karam (ed.), The Molecular Biology of Bacteriophage T4. ASM Press, Washington, DC. ISBN 1-55581-064-0
• Herskowitz, I., and F. Banuett. 1984. Interaction of phage, host, and environmental factors in governing the λ lysis-lysogeny decision, p. 59-73. In V. L. Chopra, B. C. Joshi, R. P. Sharma, and H. C. Bansal (eds.), Genetics, New Frontier: Proceedings of the XV International Congress of Genetics. Oxford and I.B.H., New Delhi.
• Lwoff, A. 1953. Lysogeny. Bacteriol. Rev. 17:269-337. full text

Phage "organismal" experimental protocols (suggested reading)

It is important to characterize phages "organismally". A number of protocols have been published. Additional phage protocols should be available before the end of 2007. Return to phage "organismal" ecology methods.

• Carlson, K. 2005. Working with bacteriophages: common techniques and methodological approaches, p. 437-494. In E. Kutter and A. Sulakvelidze (eds.), Bacteriophages: Biology and Application. CRC Press, Boca Raton, Florida. ISBN 0-8493-1336-8, Google Books
• Auad, L., and R. R. Raya. 2001. Methods for isolation and titration of bacteriophages from Lactobacillus., p. 203-208?. In J. F. T. Spencer and A. L. Ragout de Spencer (eds.), Food Microbiology Protocols. Humana Press, Totowa, New Jersey. ISBN 0-8960-3867-X, Google Books
• Carlson, K., and E. S. Miller. 1994. Enumerating phage: the plaque assay, p. 427-429. In J. D. Karam (ed.), Molecular Biology of Bacteriophage T4. ASM Press, Washington, DC. ISBN 1-55581-064-0
• Carlson, K., and E. S. Miller. 1994. General procedures, p. 427-437. In J. D. Karam (ed.), Molecular Biology of Bacteriophage T4. ASM Press, Washington, DC. ISBN 1-55581-064-0
• Carlson, K. 1994. Single-step growth, p. 434-437. In J. D. Karam (ed.), Molecular Biology of Bacteriophage T4. ASM Press, Washington. ISBN 1-55581-064-0
• Snustad, D. P., and D. S. Dean. 1971. Genetics Experiments with Bacterial Viruses. W. H. Freeman and Co., San Francisco. ISBN 0-7167-0161-8
• Eisenstark, A. 1967. Bacteriophage techniques. Methods in Virology 1:449-524.
• Adams, M. H. 1959. Bacteriophages. Interscience, New York.

Phage population ecology (suggested reading)

There are very few reviews on phage ecology that spend much time emphasizing phage population ecology, published at least. Anticipate better than a doubling of the number before the end of 2007. Return to phage population ecology.

• Abedon, S. T. 2006. Phage ecology, p. 37-46. In R. Calendar and S. T. Abedon (eds.), The Bacteriophages. Oxford University Press, Oxford. ISBN 0-19-514850-9
• Bull, J. J., D. W. Pfening, and I.-W. Wang. 2004. Genetic details, optimization, and phage life histories. Trends Ecol. Evol. 19:76-82. abstract & pay article

Phage community ecology (suggested reading)

Having received the most attention from both experimentalists and theoreticians among the various phage ecologies, a relatively large number of phage ecology reviews exist. Note that much of this literature has been motivated more from the bacterial rather than explicitly the phage perspective. See coevolution on the phage experimental evolution page for additional references. Return to phage community ecology.

• Abedon, S. T. 2006. Phage ecology, p. 37-46. In R. Calendar and S. T. Abedon (eds.), The Bacteriophages. Oxford University Press, Oxford. ISBN 0-19-514850-9
• Abedon, S. T., and J. T. LeJeune. 2005. Why bacteriophage encode exotoxins and other virulence factors. Evolutionary Bioinformatics Online 1:97-110. full text
• Comeau, A. M., and H. M. Krisch. 2005. War is peace--dispatches from the bacterial and phage killing fields. Curr. Opin. Mirobiol. 8:488-494. abstract & pay article
• Weinbauer, M. G., and F. Rassoulzadegan. 2004. Are viruses driving microbial diversification and diversity? Environmental Microbiology 6:1-11. abstract
• Levin, B. R., and J. J. Bull. 2004. Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2:166-173. abstract
• Sutherland, I. W., K. A. Hughes, L. C. Skillman, and K. Tait. 2004. The interaction of phage and biofilms. FEMS Microbiol. Lett. 232:1-6. abstract
• Bohannan, B. J. M., and R. E. Lenski. 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol. Lett. 3:362-377. full text
• Suttle, C. A. 1994. The significance of viruses to mortality in aquatic microbial communities. Microb. Ecol. 28:237-243. abstract & pay article
• Miller, R. V., and G. S. Sayler. 1992. Bacteriophage-host interactions in aquatic systems, p. 176-193. In E. M. H. Wellington and J. D. van Elsas (eds.), Genetic Interactions among Microorganisms in the Natural Environment. Pergamon Press, Oxford. ISBN 0-08-042000-1
• Lenski, R. E. 1988. Dynamics of interactions between bacteria and virulent bacteriophage. Adv. Microbial. Ecol. 10:1-44.
• Levin, B. R., and R. E. Lenski. 1985. Bacteria and phage: A model system for the study of the ecology and co-evolution of hosts and parasites, p. 227-242. In D. Rollinson and R. M. Anderson (eds.), Ecology and Genetics of Host-Parasite Interactions. Academic Press, London. ISBN 0-12-593690-7
• Krüger, D. H., and T. A. Bickle. 1983. Bacteriophage survival: Multiple mechanisms for avoiding deoxyribonucleic acid restriction systems of their hosts. Microbiol. Rev. 47:345-360. full text
• Levin, B. R., and R. E. Lenski. 1983. Coevolution in bacteria and their viruses and plasmids, p. 99-127. In D. J. Futuyama and M. Slatkin (eds.), Coevolution. Sinauer Associates, Inc., Sunderland, Massachusetts. ISBN 0-87893-229-1
• Barksdale, L., and S. B. Ardon. 1974. Persisting bacteriophage infections, lysogeny, and phage conversions. Ann. Rev. Microbiol. 28:265-299. abstract & pay article
• Anderson, E. S. 1957. The relations of bacteriophages to bacterial ecology, p. 189-217. In R. E. O. Williams and C. C. Spicer (eds.), Microbial Ecology. Cambridge University Press, London.

Phage ecosystem ecology (suggested reading)

The majority (if not all!) reviews with a phage ecosystem ecology emphasis also emphasize aquatic phage ecology. The following are examples. Return to phage ecosystem ecology.

• Weinbauer, M. G. 2004. Ecology of Prokaryotic Viruses. FEMS Microbiol. Rev. 28:127-181. abstract
• Wommack, K. E., and R. R. Colwell. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64:69-114. full text
• Suttle, C. A. 2000. Cyanophages and their role in the ecology of cyanobacteria, p. 563-589. In B. A. Whitton and M. Potts (eds.), The Ecology of Cyanobacteria: Their Diversity in Time and Space. Kluwer Academic Publishers, Boston. ISBN 0-7923-4735-8
• Suttle, C. A. 2000. The ecology, evolutionary and geochemical consequences of viral infection of cyanobacteria and eukaryotic algae, p. 248-286. In C. J. Hurst (ed.), Viral Ecology. Academic Press, New York. ISBN 0-12-362675-7
• Fuhrman, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548. abstract & pay article
• Wilhelm, S. W., and C. A. Suttle. 1999. Viruses and nutrient cycles in the sea. BioScience 49:781-788. full text
• Bratbak, G., T. F. Thingstad, and M. Heldal. 1994. Viruses and the microbial loop. Microb. Ecol. 28:209-221. abstract & pay article
• Fuhrman, J. A., R. M. Wilcox, R. T. Noble, and N. C. Law. 1993. Viruses in marine food webs, p. 295-298. In R. Guerrero and C. Pedros-Alio (eds.), Trends in microbial ecology. Spanish Society for Microbiology, Barcelona.
• Thingstad, T. F., M. Heldal, G. Bratbak, and I. Dundas. 1993. Are viruses important partners in pelagic food webs? Trends Ecol. Evol. 8:209-213. abstract
• Fuhrman, J. A. 1992. Bacterioplankton roles in cycling of organic matter: the microbial food web, p. 361-383. In P. G. Falkowski and A. D. Woodhead (eds.), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum, New York. ISBN 0-306-44192-6

Terrestrial phage ecology (suggested reading)

Not nearly as well developed as aquatic phage ecology, due to the complexity and heterogensity of solid phase versus liquid phage, terrestrial phage ecology has been explored in a number of reviews. The following are suggested readings.

• Gill, J. J., and S. T. Abedon. 2003. Bacteriophage ecology and plants. APSnet feature. full text
• Williams, S. T., A. M. Mortimer, and J. Eccleston. 1994. Bacteriophages in soil, p. 121R. Webster and A. Granoff (eds.), Encyclopedia of Virology. Academic Press.
• Williams, S. T., A. M. Mortimer, and L. Manchester. 1987. Ecology of soil bacteriophages, p. 157-179. In S. M. Goyal, C. P. Gerba, and G. Bitton (eds.), Phage Ecology. John Wiley & Sons, New York. ISBN 0-471-82419-4
• Williams, S. T., and S. Lanning. 1984. Studies of the ecology of streptomycete phage in soil, p. 473-483. In L. Ortiz-Ortiz, L. F. Bojalil, and V. Yakoleff (eds.), Biological, Biochemical and Biomedical Aspects of Actinomycetes. Academic Press, London. ISBN 0-12-528620-1
• Anderson, E. S. 1957. The relations of bacteriophages to bacterial ecology, p. 189-217. In R. E. O. Williams and C. C. Spicer (eds.), Microbial Ecology. Cambridge University Press, London.

The following deals more with phage (and other virus) retention in soils more than phage ecology per se.

• Duboise, S. M., B. E. Moore, C. A. Sorber, and B. P. Sagik. 1979. Viruses in soil systems, p. 245-285. In H. D. Isenberg (ed.), CRC Critical Reviews in Microbiology. CRC Press, Boca Raton, FL.

Aquatic phage ecology (suggested reading)

Aquatic phage ecology came to dominate phage ecology stemming from the seminal publication by Bergh et al. in 1989 (Bergh, O., K. Y. Børsheim, G. Bratbak, and M. Heldal. 1989. High abundance of viruses found in aquatic environments. Nature 340:467-468.). A large number of publications, and a large number reviews followed. The latter are listed below, exclusive of those listed above under the heading of Phage ecosystem ecology (suggested reading). See also cyanophage for additional references.

• Suttle, C.A. 2007. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5:801-812. abstract & pay article
• Mann, N. H. 2006. Phages of cyanobacteria, p. 517-533. In R. Calendar and S. T. Abedon (eds.), The Bacteriophages. Oxford University Press, Oxford. ISBN 0-471-82419-4
• Miller, R. V. 2006. Marine phages, p. 534-544. In R. Calendar and S. T. Abedon (eds.), The Bacteriophages. Oxford University Press, Oxford. ISBN 0-471-82419-4
• Brüssow, H., and E. Kutter. 2005. Phage ecology, p. 129-164. In E. Kutter and A. Sulakvelidze (eds.), Bacteriophages: Biology and Application. CRC Press, Boca Raton, Florida. ISBN 0-8493-1336-8
• Paul, J. H., and M. B. Sullivan. 2005. Marine phage genomics: what have we learned? Curr. Opin. Biotechnol. 16:299-307. abstract & pay article
• Fuhrman, J. A., and M. Schwalbach. 2003. Viral influence on aquatic bacterial communities. Biol. Bull. 204:192-195. full text
• Paul, J. H., M. B. Sullivan, A. M. Segall, and F. Rohwer. 2002. Marine phage genomics. Comparative Biochemistry and Physiology 133:463-476.
• Suttle, C. A. 2002. Community structure: viruses, p. 364-370. In C. J. Hurst, G. R. Knudson, M. J. McInerney, L. D. Stezenbach, and M. V. Walter (eds.), Manual of Environmental Microbiology (2nd Edition). ASM Press, Washington, DC.
• Fuhrman, J. A. 2000. Impact of viruses on bacterial processes, p. 327-350. In D. L. Kirchman (ed.), Microbial Ecology of the Oceans. Wiley & Sons, New York.
• Martin, E. L., and T. A. Kokjohn. 1999. Cyanophages, p. 324-332. In A. Granoff and R. G. Webster (eds.), Encyclopedia of Virology second edition. Academic Press, San Diego.
• Suttle, C. A. 1999. Do viruses control the oceans? Nat. His. 108:48-51.
• Proctor, L. M. 1998. Marine virus ecology, p. 113-130. In S. E. Cooksey (ed.), Molecular Approaches to the Study of the Ocean. Chapman & Hall, London.
• Proctor, L. M. 1997. Advances in the study of marine viruses. Microscopy Research and Technique 37:136-161.
• Suttle, C. A. 1997. Community structure: viruses, p. 272-277. In C. J. Hurst, G. R. Knudson, M. J. McInerney, L. D. Stezenbach, and M. V. Walter (eds.), Manual of Environmental Microbiology. ASM Press, Washington DC.
• Paul, J. H., C. A. Kellogg, and S. C. Jiang. 1996. Viruses and DNA in marine environments, p. 119-128. In R. R. Colwell, U. Simidu, and K. Ohwada (eds.), Microbial Diversity in Time and Space. Plenum Press, New York, N.Y.
• Suttle, C. A. 1994. The significance of viruses to mortality in aquatic microbial communities. Microb. Ecol. 28:237-243.
• Bratbak, G., M. Heldal, A. Naess, and T. Roeggen. 1993. Viral impact on microbial communities, p. 299-302. In R. Guerrero and C. Pedros-Alio (eds.), Trends in Microbial Ecology. Spanish Society for Microbiology, Barcelona.
• Fuhrman, J. A., and C. A. Suttle. 1993. Viruses in marine planktonic systems. Oceanography 6:50-62.
• Thingstad, T. F., M. Heldal, G. Bratbak, and I. Dundas. 1993. Are viruses important partners in pelagic food webs? Trends Ecol. Evol. 8:209-213.
• Miller, R. V., and G. S. Sayler. 1992. Bacteriophage-host interactions in aquatic systems, p. 176-193. In E. M. H. Wellington and J. D. van Elsas (eds.), Genetic Interactions among Microorganisms in the Natural Environment. Pergamon Press, Oxford.
• Cannon, R. E. 1987. Cyanophage ecology, p. 245-265. In S. M. Goyal, C. P. Gerba, and G. Bitton (eds.), Phage Ecology. John Wiley & Sons, New York.
• Farrah, S. R. 1987. Ecology of phage in freshwater environments, p. 125-136. In S. M. Goyal, G. P.
• Moebus, K. 1987. Ecology of marine bacteriophages, p. 137-156. In S. M. Goyal, G. P. Gerba, and G. Bitton (eds.), Phage Ecology. John Wiley & Sons, New York.
• Cannon, R. E., M. S. Shange, and E. DeMichele. 1974. Ecology of blue-green algal viruses. J. Environ. Eng. Div. , ASCE 100:1205-1211.
• Shilo, M. 1972. The ecology of cyanophages. Bamidgeh 24:76-82.
• Spencer, R. 1963. Bacterial viruses in the sea, p. 350-365. In C. H. Oppenheimer (ed.), Symposium on Marine Microbiology. Charles C. Thomas, Publisher, Springfield, IL.

Other environments (suggested reading)

• Bogosian, G. 2006. Control of bacteriophage contamination in commercial microbiology and fermentation facilities, p. 667-673. In R. Calendar and S. T. Abedon (eds.), The Bacteriophages. Oxford University Press, Oxford. ISBN 0-195-14850-9, Google Books

• Stedman, K. M., A. Clore, and Y. Combet-Blanc. 2006. Biogeographical diversity of archaeal viruses, p. 131-144?. In N. A. Logan, H. M. Lappin-Scott, and P. C. F. Oyston (eds.), Prokaryotic Diversity: Mechanisms and Significance. Cambridge University Press, Cambridge, UK. ISBN 0-521-86935-8, Google Books

• Moineau, S., and C. Lévesque. 2005. Control of bacteriophages in industrial ferments, p. 285-296. In E. Kutter and A. Sulakvelidze (eds.), Bacteriophages: Biology and Application. CRC Press, Boca Raton, Florida. ISBN 0-8493-1336-8

• Sanders, M. E. 1987. Bacteriophages of industrial importance, p. 211-244. In S. M. Goyal, G. P. Gerba, and G. Bitton (eds.), Phage Ecology. John Wiley & Sons, New York. ISBN 0-471-82419-4

Notes

1. ^ The term "prokaryotes" is useful to mean the sum of the bacteria and archaeabacteria but otherwise can be controversial, as discussed by Woese, 2004; see also pp. 103-104 of Woese, C. R. 2005. Evolving biological organization, p. 99-118. In J. Sapp (ed.), Microbial Phylogeny and Evolution Concepts and Controversies. Oxford University Press, Oxford. A history of the concept is provided by Sapp, 2006.
2. ^ This article on phage ecology was expanded from a stub during the writing of the first chapter of the edited monograph, Bacteriophage Ecology (forecasted publication date: March, 2008, Cambridge University Press), in order to be cited by that chapter especially as a repository of phage ecology review chapters and articles.
3. ^ Pseudolysogeny references: Barksdale, L., and S. B. Ardon. 1974. Persisting bacteriophage infections, lysogeny, and phage conversions. Ann. Rev. Microbiol. 28:265-299; Miller, R. V., and S. A. Ripp. 2002. Pseudolysogeny: A bacteriophage strategy for increasing longevity in situ, p. 81-91. In M. Syvanen and C. I. Kado (eds.), Horizontal Gene Transfer. Academic Press, San Diego.
4. ^ Summers, W. C. 1991. From culture as organisms to organisms as cell: historical origins of bacterial genetics. J. Hist. Biol. 24:171-190.
5. ^ Many PDF- (or, alternatively, html-) based articles are online through PubMed or via the web sites of open access journals such as those published by BioMed Central. Alternativley, they may be posted on "private" web sites (perhaps in copyright violation) by authors or other individuals. Consequently, it is often possible to find an article by doing a Google search on article titles. You can sometimes increase useful hits by placing titles in quotes, adding author last names (outside of quotes), or by limiting searches to PDF documents.