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Phage ecology

From Wikipedia, the free encyclopedia
Interaction of bacteriophages with their environments

Bacteriophages (phages), potentiallythe most numerous "organisms" on Earth, are theviruses ofbacteria (more generally, ofprokaryotes[1]).Phage ecology is the study of the interaction ofbacteriophages with theirenvironments.[2]

Introduction to phage ecology

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Vastness of phage ecology

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Phages areobligate 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 (callednormal flora). Often these bacteria are found in large numbers. As a consequence, phages are found almost everywhere.[citation needed]

As arule of thumb, many phage biologists expect that phagepopulation densities will exceed bacterial densities by a ratio of 10-to-1 or more (VBR or virus-to-bacterium ratio; see[3] for a summary of actual data). As there exist estimates of bacterial numbers on Earth of approximately 1030,[4] there consequently is an expectation that 1031 or more individual virus (mostly phage[5]) particles exist[1], making phages the most numerous category of "organisms" on our planet.

Bacteria (along witharchaea) appear to be highly diverse and there possibly are millions of species.[6] 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,[7] and also individualphage types[8]

Studying phage ecology

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The study of phage ecology reflects established scientific disciplines in ecological studies in scope, the most obvious being generalecology. Accordingly, phage ecology is treated under the following heads—"organismal" ecology,population ecology,community ecology, andecosystem ecology. Phage ecology also may be considered (though mostly less well formally explored) from perspectives of phagebehavioral ecology,evolutionary ecology,functional ecology,landscape ecology, mathematical ecology,molecular ecology, physiological ecology (or ecophysiology), andspatial ecology. Phage ecology additionally draws (extensively) frommicrobiology, particularly in terms ofenvironmental microbiology, but also from an enormous catalog (90 years) of study ofphage and phage-bacterial interactions in terms of theirphysiology and, especially, theirmolecular biology.[citation needed]

Phage "organismal" ecology

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Phage "organismal" ecology is primarily the study of theevolutionary 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 torestriction
    • resistance to abortive infection
  • varioustemperate-phage properties, including
  • the tendency of at least some phage to enter into (and then subsequently leave) a not very well understood state known (inconsistently) as pseudolysogeny[9][10]

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 classicalmolecular andmolecular genetic analyses of bacteriophage.

From the perspective ofecological subdisciplines, we can also consider phagebehavioral 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 ofphage experimental adaptation studies.

Historical overview

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In the mid 1910s, when phage were first discovered, the concept of phage was very much awhole-culture phenomenon (like much of microbiology[11]), where various types of bacterial cultures (onsolid media, inbroth) were visibly cleared by phage action. Though from the start there was some sense, especially byFėlix d'Hėrelle, that phage consisted of individual "organisms", in fact it wasn't until the late 1930s through the 1940s that phages were studied, with rigor, as individuals, e.g., byelectron microscopy and single-step growth experiments.[12] 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.[citation needed]

This somewhat whole-organismal view of phage biology saw its heyday during the 1940s and 1950s, before giving way to much morebiochemical,molecular genetic, andmolecular biological analyses of phages, as seen during the 1960s and onward. This shift, paralleled in much of the rest of microbiology[2], represented a retreat from a much more ecological view of phages (first as bacterial killers, and then asorganisms 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 molecularmodel systems.[citation needed]

Methods

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The basic experimental toolkit of phage "organismal" ecology consists of the single-step growth (or one-step growth;[12]) experiment and the phageadsorption curve.[13] Single-step growth is a means of determining the phagelatent 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'sburst size, which is the number of phage (on average) that are produced per phage-infected bacterium.[citation needed]

The adsorption curve is obtained by measuring the rate at which phagevirion particles (seeVirion#Structure) attach to bacteria. This is usually done by separating free phage from phage-infectedbacteria 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.[citation needed]

Phage population ecology

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Apopulation is a group ofindividuals which either do or caninterbreed or, if incapable of interbreeding, then are recently derived from a single individual (aclonal 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 includecompetition as well ascooperation. Competition can be either in terms of rates ofpopulation growth (as seen especially at lower population densities in resource-rich environments) or in terms of retention ofpopulation sizes (seen especially at higher population densities where individuals are directly competing overlimited resources). Respectively, these arepopulation-density independent and dependent effects.[citation needed]

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

Phage community ecology

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Acommunity consists of all of the biologicalindividuals found within a given environment (more formally, within anecosystem), particularly when more than onespecies 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 singlepopulation. 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, withpredator-prey interactions). An important consequence of these interactions iscoevolution.

Relationship with bacteria

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The interaction of phage withbacteria is the primary concern of phage community ecologists. Bacteria have developed mechanisms that prevent phages from having an effect on them, which has led to thisevolutionary arms race between the phages and their host bacteria.[14]Bacterial resistance to phages puts pressure on the phages to develop stronger effects on the bacteria. TheRed Queen hypothesis describes this relationship, as the organisms must constantly adapt and evolve in order to survive.[15] This relationship is important to understand as phages are now being used for more practical and medicinal purposes.

Bacteria have developed multiple defense mechanisms to fight off the effects of bacteriophages.[16] In experimentation, amount of resistance can be determined by how much of a plate (generallyagar with bacteria, infected with phages) ends up being clear. The clearer, the less resistant as more bacteria have beenlysed.[17] The most common of these defense mechanisms is called therestriction-modification system (RM system). In this system, foreign DNA trying to enter the bacterial host is restricted byendonucleases that recognize specific base pairs within the DNA, while the DNA of the cell is protected from restriction due tomethylase.[16] RM systems have evolved to keep up with the ever-changing bacteria and phage. In general, these RM types differ in the nucleotide sequences that they recognize.[18] However, there is an occasional slip where the endonuclease misses the DNA sequence of the phage and the phage DNA is able to enter the cell anyway, becoming methylated and protected against the endonuclease. This accident is what can spur the evolution of the RM system. Phages can acquire or use the enzyme from the host cell to protect their own DNA, or sometimes they will have proteins that dismantle the enzyme that is meant to restrict the phage DNA.[16] Another option is for the phage to insert different base pairs into its DNA, thereby confusing the enzyme.

Another mechanism employed by bacteria is referred to asCRISPR. This stands for “clustered regularly interspersed palindromic repeats” which means that the immunity to phages by bacteria has been acquired via adding spacers of DNA that are identical to that of the DNA from the phage. Some phages have been found to be immune to this mechanism as well. In some way or another, the phages have managed to get rid of the sequence that would be replicated.

A third way that bacteria have managed to escape the effects of bacteriophages is byabortive infection. This is a last resort option- when the host cell has already been infected by the phage. This method is not ideal for the host cell, as it still leads to its death. The redeeming feature of this mechanism is the fact that it interferes with the phage processes and prevents it from then moving on to infect other cells.[16]

On top of the above mentioned strategies, a growing arsenal of anti-phage immune systems has been described and quantified in bacteria.[19]

Phages are also capable of interacting with species other than bacteria, e.g., such as phage-encodedexotoxin interaction withanimals.[20]Phage therapy is an example of applied phage community ecology.[citation needed]

Phage ecosystem ecology

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Anecosystem consists of both thebiotic andabiotic components of an environment. Abiotic entities are not alive and so an ecosystem essentially is acommunity combined with the non-living environment within which that ecosystem exists.Ecosystem ecology naturally differs fromcommunity ecology in terms of the impact of the community on these abiotic entities, andvice versa. In practice, the portion of the abiotic environment of most concern to ecosystem ecologists isinorganicnutrients andenergy.

Phages impact the movement of nutrients and energy within ecosystems primarily bylysing bacteria. Phages can also impact abiotic factors via the encoding of exotoxins (a subset of which are capable of solubilizing thebiological tissues of livinganimals[3]). Phage ecosystem ecologists are primarily concerned with the phage impact on the globalcarbon cycle, especially within the context of a phenomenon known as themicrobial loop.

Notes

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  1. ^The term "prokaryotes" is useful to mean the sum of thebacteria andarchaea but otherwise can be controversial, as discussed byWoese CR (June 2004)."A new biology for a new century".Microbiol. Mol. Biol. Rev.68 (2):173–86.doi:10.1128/MMBR.68.2.173-186.2004.PMC 419918.PMID 15187180.; see also pp. 103–4 ofSapp, Jan (2004). "Evolving biological organization".Microbial phylogeny and evolution: concepts and controversies. Oxford [Oxfordshire]: Oxford University Press. pp. 99–118.ISBN 978-0-19-516877-8.
    Sapp J (September 2006)."Two faces of the prokaryote concept"(PDF).Int. Microbiol.9 (3):163–72.PMID 17061206. provides a history.
  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 ofphage ecology review chapters and articles.
  3. ^Weinbauer MG (May 2004)."Ecology of prokaryotic viruses".FEMS Microbiol. Rev.28 (2):127–81.doi:10.1016/j.femsre.2003.08.001.PMID 15109783.
  4. ^Whitman WB, Coleman DC, Wiebe WJ (June 1998)."Prokaryotes: the unseen majority".Proc. Natl. Acad. Sci. U.S.A.95 (12):6578–83.Bibcode:1998PNAS...95.6578W.doi:10.1073/pnas.95.12.6578.PMC 33863.PMID 9618454.
  5. ^Wommack KE, Colwell RR (March 2000)."Virioplankton: viruses in aquatic ecosystems".Microbiol. Mol. Biol. Rev.64 (1):69–114.doi:10.1128/MMBR.64.1.69-114.2000.PMC 98987.PMID 10704475.
  6. ^Curtis TP, Sloan WT, Scannell JW (August 2002)."Estimating prokaryotic diversity and its limits".Proc. Natl. Acad. Sci. U.S.A.99 (16):10494–9.Bibcode:2002PNAS...9910494C.doi:10.1073/pnas.142680199.PMC 124953.PMID 12097644.
  7. ^Sogin ML, Morrison HG, Huber JA, et al. (August 2006)."Microbial diversity in the deep sea and the underexplored "rare biosphere"".Proc. Natl. Acad. Sci. U.S.A.103 (32):12115–20.Bibcode:2006PNAS..10312115S.doi:10.1073/pnas.0605127103.PMC 1524930.PMID 16880384.
  8. ^Breitbart M, Salamon P, Andresen B, et al. (October 2002)."Genomic analysis of uncultured marine viral communities".Proc. Natl. Acad. Sci. U.S.A.99 (22):14250–5.Bibcode:2002PNAS...9914250B.doi:10.1073/pnas.202488399.PMC 137870.PMID 12384570.
  9. ^Barksdale L, Arden SB (1974). "Persisting bacteriophage infections, lysogeny, and phage conversions".Annu. Rev. Microbiol.28:265–99.doi:10.1146/annurev.mi.28.100174.001405.PMID 4215366.
  10. ^Miller, R. V. & S. A. Ripp (2002). "Pseudolysogeny: A bacteriophage strategy for increasing longevity in situ". In Kado, Clarence I. & Syvanen, Michael (eds.).Horizontal gene transfer (2nd ed.). Boston: Academic Press. pp. 81–91.ISBN 978-0-12-680126-2.
  11. ^Summers WC (1991). "From culture as organism to organism as cell: historical origins of bacterial genetics".J Hist Biol.24 (2):171–90.doi:10.1007/bf00209428.PMID 11612551.S2CID 36544748.
  12. ^abYou L, Suthers PF, Yin J (April 2002)."Effects of Escherichia coli physiology on growth of phage T7 in vivo and in silico".J. Bacteriol.184 (7):1888–94.doi:10.1128/JB.184.7.1888-1894.2002.PMC 134924.PMID 11889095.
  13. ^Abedon ST, Hyman P, Thomas C (December 2003)."Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability".Appl. Environ. Microbiol.69 (12):7499–506.Bibcode:2003ApEnM..69.7499A.doi:10.1128/AEM.69.12.7499-7506.2003.PMC 310036.PMID 14660403.
  14. ^Stern, Adi; Sorek, Rotem (2011)."The phage-host arms race: Shaping the evolution of microbes".BioEssays.33 (1):43–51.doi:10.1002/bies.201000071.PMC 3274958.PMID 20979102.
  15. ^Lenski, Richard E.; Levin, Bruce R. (1 January 1985). "Constraints on the Coevolution of Bacteria and Virulent Phage: A Model, Some Experiments, and Predictions for Natural Communities".The American Naturalist.125 (4):585–602.doi:10.1086/284364.JSTOR 2461275.S2CID 82562085.
  16. ^abcdISSN 0265-9247 issue v33i0001 article 43
  17. ^Buckling, Angus; Rainey, Paul B. (1 January 2002)."Antagonistic Coevolution between a Bacterium and a Bacteriophage".Proceedings: Biological Sciences.269 (1494):931–936.doi:10.1098/rspb.2001.1945.JSTOR 3067783.PMC 1690980.PMID 12028776.
  18. ^ISSN 0092-8240 issue v62i0004 article 759
  19. ^Beavogui, Angelina; Lacroix, Auriane; Wiart, Nicolas; Poulain, Julie; Delmont, Tom O.; Paoli, Lucas; Wincker, Patrick; Oliveira, Pedro H. (2024-03-08)."The defensome of complex bacterial communities".Nature Communications.15 (1).doi:10.1038/s41467-024-46489-0.ISSN 2041-1723.PMC 10924106.
  20. ^"Evolutionary Bioinformatics Online 2005". Libertas Academica. Archived fromthe original on 2006-05-26.

External links

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General
Producers
Consumers
Decomposers
Microorganisms
Food webs
Example webs
Processes
Defense,
counter
Ecology:Modelling ecosystems: Other components
Population
ecology
Species
Species
interaction
Spatial
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