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Bacteriophages(phages), potentiallythe most numerous "organisms" on Earth,are thevirusesofbacteria(more generally, ofprokaryotes[1]).Phage ecologyis the study of the interaction ofbacteriophageswith theirenvironments.[2]

Introduction to phage ecology[edit]

Vastness of phage ecology[edit]

Phages areobligate intracellular parasitesmeaning 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 densitieswill 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 1031or 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[edit]

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 ofphageand phage-bacterial interactions in terms of theirphysiologyand, especially, theirmolecular biology.[citation needed]

Phage "organismal" ecology[edit]

Phage "organismal" ecology is primarily the study of theevolutionary ecologicalimpact 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
  • adsorptionconstant, plus
    • rates of virion diffusion
    • virion decay (inactivation) rates
  • host range,plus
    • resistance torestriction
    • resistance to abortive infection
  • varioustemperate-phageproperties, 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 classicalmolecularandmolecular geneticanalyses 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 adaptationstudies.

Historical overview[edit]

In the mid 1910s, when phage were first discovered, the concept of phage was very much awhole-culturephenomenon (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 microscopyand 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 biologicalanalyses 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 asorganismsunto 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[edit]

The basic experimental toolkit of phage "organismal" ecology consists of the single-step growth (or one-step growth;[12]) experiment and the phageadsorptioncurve.[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 phagevirionparticles (seeVirion#Structure) attach to bacteria. This is usually done by separating free phage from phage-infectedbacteriain 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[edit]

Apopulationis a group ofindividualswhich either do or caninterbreedor, if incapable of interbreeding, then are recently derived from a single individual (aclonal population).Population ecologyconsiders 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 includecompetitionas 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-densityindependent 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 phageadsorban individual bacterium.

Phage community ecology[edit]

Acommunityconsists of all of the biologicalindividualsfound within a given environment (more formally, within anecosystem), particularly when more than onespeciesis present.Community ecologystudies 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[edit]

The interaction of phage withbacteriais 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 racebetween the phages and their host bacteria.[14]Bacterial resistanceto phages puts pressure on the phages to develop stronger effects on the bacteria. TheRed Queen hypothesisdescribes 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 (generallyagarwith 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 byendonucleasesthat 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-encodedexotoxininteraction withanimals.[20]Phage therapyis an example of applied phage community ecology.[citation needed]

Phage ecosystem ecology[edit]

Anecosystemconsists of both thebioticandabioticcomponents of an environment. Abiotic entities are not alive and so an ecosystem essentially is acommunitycombined with the non-living environment within which that ecosystem exists.Ecosystem ecologynaturally differs fromcommunity ecologyin 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 isinorganicnutrientsandenergy.

Phages impact the movement of nutrients and energy within ecosystems primarily bylysingbacteria. Phages can also impact abiotic factors via the encoding of exotoxins (a subset of which are capable of solubilizing thebiological tissuesof 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[edit]

  1. ^The term "prokaryotes"is useful to mean the sum of thebacteriaandarchaeabut 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.PMC419918.PMID15187180.The Dismantling of Bacteriology and a Deconstruction of the Procaryote{{cite journal}}:External link in|quote=(help);see also pp. 103–4 of Sapp, Jan (2004). "Evolving biological organization".Microbial phylogeny and evolution: concepts and controversies.Oxford [Oxfordshire]: Oxford University Press. pp.99–118.ISBN978-0-19-516877-8.
    Sapp J (September 2006)."Two faces of the prokaryote concept"(PDF).Int. Microbiol.9(3): 163–72.PMID17061206.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.PMID15109783.
  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.PMC33863.PMID9618454.
  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.PMC98987.PMID10704475.
  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.PMC124953.PMID12097644.
  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.PMC1524930.PMID16880384.
  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.PMC137870.PMID12384570.
  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.PMID4215366.
  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.ISBN978-0-12-680126-2.
  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.PMID11612551.S2CID36544748.
  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.PMC134924.PMID11889095.
  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.PMC310036.PMID14660403.
  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.PMC3274958.PMID20979102.
  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.JSTOR2461275.S2CID82562085.
  16. ^abcdISSN0265-9247issue 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.JSTOR3067783.PMC1690980.PMID12028776.
  18. ^ISSN0092-8240issue 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.ISSN2041-1723.PMC10924106.
  20. ^"Evolutionary Bioinformatics Online 2005".Libertas Academica. Archived fromthe originalon 2006-05-26.

External links[edit]

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