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    Parashar 2015. Interspecies Communication in Oral Biofilm - An Ocean of Information - Elsevier Enhanced Reader

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    Parashar 2015. Interspecies communication in oral

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    ‘ral Science nerationa 12 (2015) 37-42 Contents lists available at ScienceDirect Oral Science International journal homepage: www.elsevier.com/locate/osi Review Interspecies communication in oral biofilm: An ocean of information Qe Amit Parashar, Shashi Parashar”, Abhishek Zingade’, Shikha Gupta‘, Sheetal Sanikop* + Deparment of Perlodomis KLE VE Instat of Dental Slenes, Belgaum P5010, Kanaan ® nsion of Urology. Defence ED Establishment (DRDE| fats Road, Gwar PIN -174002. MP nda «Doparment of edadonts. People antl Academy. Pope Univers. pa. a ARTICLE INFO ABSTRACT Received 25 August 2014, Received in ceed fot 13 December 2014 ‘Accepted 5 Febery 2015 ‘The diversity of signalling opportunities within microbial communities, and the sgaliant role ofthese molecules in coordinating gene expression and promoting biofilm formation, has provided the imp tus to investigate the potential of inhibitory analogues to disrupt chese networks, thercby providing mechanisms to control or influence the development of dental plague. Within the oral bili. es ‘dent bacterial cells interact with one another and exchange messages in the form of signalling molecules ‘and metabolites. In his review article, our aim Isto elaborate the role ofthis quarum sensing and tele — Imvlvment in paingenesisodeiher infrmatin iat an be stl opt ptivay fo onal = ©2015 apne Stomatol Soy. Pulsed by Eve Al gh reseed Contents 1. Invodction os o a” 2 Rules of engagement dining bacterial communication 38 3. Costand specie fete signaling x9 4. Mechonims of communications. oo co on SOI 39 4.1. Alin spatiotemporal dcvclopment of mutspedes communis a 5. Faure perspectives ai 8 Concasions : : : ai Git "The Great Bacterial et communication ad development in rl bins oS at Conti ofinerest 2 Source of nding 2 References 2 1. Introduction voids permeating densely packed microcolonies, lke roads and ‘An adherent microbial population that is embedded in and attached to surfaces or interfaces is known as a biofilm (|. Mature dental biofilms consist of towering microcolonies in which the resident bacterial cells interact with one another and exchange messages in the form of signalling molecules and metabolites Biofilms have been likened to miniature cities, with channels and * Covresponding author. Te: 91 9685480824. mal adress captatparasharégmalcom (A Paresh. pot ong 10.1016951388-8543(15)0016-6 alleys running between tall buildings (2) ‘The foundations of dental plaque are laid by the primary colo- nizers, predominantly streptococci, Actinomyces and a few other genera, which provide binding sites for co-adhesion with other bacteria [3]. the bioflm grows in complexity, diferent microen- vironments are formed within, and new niches are provided for later colonizers Initial colonizers such as streptococci (yellow) and Actinomyces (blue) bind to the salivary pellicle, which coats the ‘enamel, and subsequently grow together with Veifonelia (purple) as multispecies biofilm communities (Fig. 1) [41 ‘Throughout the development of dental plaque, adherent bacte- ria sense their neighbours and make appropriate responses. Some 1388-8613/0 2015 Japanese Stomatologicl Society Publshedby Elsevier Ld lights reserved, 8 A Parashar 0, / nS nermaonl 12 (2015) 7-42 Tooth safice Fig 1. ral ace colonization: Aigute showing model for oral ceva clonzatio of mainly two types: ery and lite colonizers, Ely colniers fst ind to he Salivary pele on the woth surface. All hese ateracons led tothe formation of dental plaques Flom the btm, tal coloizts ad ate clonzers ae detaled by the ‘tganiss name athe righ side af the gue (of these interactions involve signalling molecules that appear to have evolved specifically o elicit responses in neighbouring bacte- ria, In other cases, bacteria sense changes in their environment that are brought about by microbial metabolism in the otal biofilm. Understanding the adaptations that bacteria undergo to prosper in mixed-species communities such as dental plague promises to ‘open new leads for controlling microbial biofiIms [5] Rules of engagement: defining bacterial communication The complexity and sheer number of microbial interactions are staggering. They can be mutually beneficial, altruistic, antag fonistic and even spiteful. Bacteria communicate via diffusible signalling molecules and by gene transfer: bacteria can also engage in erosstal if in contact with host cells (Fig. 2) [6]. Some require Amtagonis: (e.g.bacteriocing)—— > Cell density- dependent signalling (e.g. via CSP; Al-2) wo Gene transfer ig.2 Schomaicrpreseranonaftherypesofimeracton: figure showinga dete eepesenationoftheiteactionofmirobiaspeces Bacteria adhereby adhesin-receptor Interactions to the acquired pele oo already attached ees (oradhesion Hacer. aterat spetgsicall) to metabolize comple host molecules, and food webs can develop, enabling the efent cing of nutrients. Bacteria commana a faible signalling molecules and by gee transfer acter can aso engage in crosstalk ifn oniat wih host cell Cell in bons ar ess sseeple to antiverobial agents aa the hast defences ths may be because of psi properties of the bin a protection fam aighbouring cl, for example, because af the sereton of netalzng enzymes to making Sense cells appear resstan (),ofllowing hoszonal ene eater The entisonmental beterogenety generated within bibl encouases genotypic and phenotypic Gaver, which enhances the ability to persist he fae ff assaul fom the mate and adapave immune espenses, fom antimicrobal tack and fom environmental sss, A Porth o/s Slenc tomato 12205) 37-42 » © Emitter © Responder) °—> 0° Signal ‘Threshcid concentration Signal concentration Time (growth) ig. 3. Coneicscteme or quorum sersing: figure showing the exponential growth cue between signal concentrations i the outer environment effet of bin, formation. As colonization occurs by early and late colonizers, emitence signa production also increases, which poste affects responder signals As the eo ‘nization increases, the sina production cases the tesa limit intimate contact or contact via structures such as nanotubes, anopods or diffusion of membrane vesicles. Teseinteractionscan ‘occur within species, between species and even between domains, Moreover, intercellular interactions are mediated by a continually expanding set of diffusible molecules (7) ‘Communication, in which one organism emits a signal and anather organism responds, therefore implies that both organisms ‘gain compensatory benefit for these potentially costly behaviours, A signal, as defined by the evolutionary biologist John Maynard Smith, is “any act or structure which alters the behaviour of other ‘organisms, which evolved because ofthat effect, and whichis effec tive because the receiver's response has also evolved.” [8], Thus, for an emission to be a signal, it must not only elicit a response in the receiving organism but also have evolved primarily to do so. More ‘often than not, a chemical interaction between two species does not provide. bidirectional benefit. Terminology has therefore been proposed for describing such non-signallinginteractions ~‘cue' and ‘coercion’. A cue refers to an emission that provides information to 2a receiver but which did not evolve explicitly for that purpose ‘The receiver benefits from responding to cue, but the emitter experiences neither an increase nor a decrease in fitness, Coercion refers to the scenario in which a substance induces a detrimental Fesponse in a receiver to the benefit ofthe emitter 3. Cost and specificity of cell-cell signalling ‘Quorum sensing (QS) or cell-cell communication is a process ‘of chemical communication among bacteria: itis defined as gene expression in response to cell density, which influences various functions, that is, virulence, acid tolerance and biofilm formation. Because bacteria within biofilms reach a high cell density, QS is considered one of the important bactetial functions [9]. Cell-cell signalling results from the production of signalling molecules by emitter cells and their accumulation in the Surrounding environ- ment. At some threshold concentration, the signalling molecules bind to receptors on or in the bacterial cell, leading t0 changes in gene expression inthe responding cell (Fig. 3) [10]. In biofilms, the process of bacteria producing signalling molecules, transporting, sensing and controlling a series of acts is called a quorum-sensing (Q5) system. QS systems control a ‘wide range of responses, including bacterial sutface adhesion, ‘extracellular matrix production, synthesis of biosurfactants, spore formation, competency, bioluminescence, virulence factor expres- sion, etc. QS systems are highly specific and accurate, which are the basisof precise regulations ofthe different bacterial phenotypes 4) Currently, there are three well-defined classes of molecules that serve as the patadigms for chemical signalling in bacte- sia: oligopeptides, acylated homoserine lactones (AliLs) and the ‘LuxS autoinducer-2 (AI-2) clas [11]. These three systems will be considered from an evolutionary perspective in particular in terms ‘of the two key components of communication: the cost associated ‘with signalling and information specificity. Costs are primarily the ‘metabolic burden that is associated with signal production, The specificity ofthe signal produced isin part a measure ofthe infor- ‘mation content of the signal, and specificity generally correlates ‘with the cost of production. The frst of the cell-cell-signalling mechanisms is oligopeptide ‘signaling, which isthe predominant signal used by Gram-positive bacteria. Typically, a preprotein is generated, processed into the active signalling peptide and exported from the cel. The biochemi- cal cost of synthesis is relatively expensive, even for short peptides. The chemical structure of the signal is precisely defined by the sequence of amino acids (1, The oligopeptide signals are highly specific, sometimes allowing distinct signalling within different strains of the same species. The second established paradigm in cell-cell signalling is ‘through AHILs. In Gram-negative bacteria, the production of AHLS involves the reaction of S-adenosyimethionine (SAM) with an acyl-acyl carrier protein (acyl-ACP), which is typically carried out by an enzyme of the Lux! family. Acyl-ACP molecules are inter~ _mediates in faty acid biosynthesis, Both these substrates have an associated metabolic burden for synthesis, and there isan interme- diate cost associated with production, The specificity ofthis system is only moderate [17]. The third cell-cell-signalling system in bacteria is generally referted to as the Luxs/Al-2 pathway. This system is found in ‘many Gram-negative and Gram-positive bacteria. The signal that is produced by al strains is thought to be an identical product (4.5- dihydroxy-2,3-pentanedione DPD))thatis inchemical equilibrium ‘withseveral furanones. Thispathway isnot specificatall,andthere- {ore it cannot convey precise information, laterestingly, this is also ‘the pathway that is associated with the lowest cost of production (19), ‘4, Mechanisms of communication Various signalling molecules and metabolic cues are involved in interspecies metabolic communication between oral bacteria | Signalling molecules: Two classes of molecules produced by oral bacteria have been implicated as true signals, produced specif- ically for the purposes of cell-to-cell communication. These are competence-stimulating peptides (CSPs), synthesized by Gram- Positive bacteria such as streptococci, and Al-2. There is some debate regarding the status of A-2 as a true signal because this ‘molecule appears to have a primary role in metabolism in atleast some bacteria [24]. Nevertheless, the widespread changes in gene expression induced by Al-2, combined with its apparent activity at extremely low concentrations (in the orderof tens of nanomolars or Jess), are consistent with a role in signalling. Al-2 and CSPs appear to be involved in intraspecies QS. However, there is accumulating evidence that they are also involved in a variety of interspecies interactions between bacteria (Fig. 4) [11 (SPs re short peptides, approximately 17-21 amino acids, pro- duced by many streptococci from the proteolytic digestion of the com¢ gene product. Historically, CSPs have been considered species-specific or even strain-specific signals. CSPs have diverse effects on oral streptococci, including. promoting competence, biofilm formation and DNA release |12|-Recent evidence hasshown that CSP can induce alarmones, which are intracellular signal molecules and are produced due to harsh environmental factors, 0 A Parashar 0, / nS nermaonl 12 (2015) 7-42 ig Comparison of especies slgnalng putvaysivlving competence sulting peptides (CPs) and autoinducer 2 (Al-2): A Bguce showing the effect of CSP and Sutoinducer2signallag pathway on bio formation Al2-poducing bacteria ae the man pat of the rl biofilm affecting CSP production by providing competence. ‘dion. production of becteiacins interes with CSP prducson Several independent mechanisms are shown nthe Ure and can convey sophisticated messages in a population including the induction of altruistic celular suicide under stressful canditions [13], CSP isa small molecule that induces bacteria into compe- tence, following which the bacteria can obtain exogenous DNA and ‘change genetic information| 14). CSP is synthesized in the cell and released into the extracellular medium, mediating the QS system. ‘When the bacterial density ofthe bioflm increases, CSP molecules in the external environment reach a certain numerical threshold ‘concentration and begin to regulate bacterial density [15]. CSP can regulate the physiological activities of Streptococcus mutans, includ- ing biofilm formation, generation of bacteriocins, stress response, acid tolerance, genetic conversion, etc. CSP signalling molecules are highly species-specific. A CSP produced by one bacterium rarely interferes with the activity of CSP produced by adifferent bacterium is}. Al2issofarthe only signalling molecule found to be widespread among both Gram-positive and Gram-negative bacteria [17]. AF-2 is a product of the activated methyl cycle, generated by LuxS- mediated cleavage of the intermediate S-ribosyihomocysteine 10 homocysteine and DPD | 18]. In solution, DPD dissociates into sev- feral forms that are collectively known as Al-2. The luxS gene, ‘encoding S-adenosylhomocysteinase (LuxS), is present in the ‘genome sequences of many oral bacteria. Six different genera of oral bacteria have been shown to pro- ‘duce Al-2 at sufficient levels for detection using a Vibrio harveyi luminescence-based bioassay [19]. Detection of Al-2 by bacteria leads to profound changes in gene expression. Many bacteria that respond to Al-2also produce it, and therefore Al-2 may function as an intraspecies signal. However, there is evidence that Al-2 is also important for interspecies interactions in microbial communities. ‘A screen of oral bacteria for Al-2 production found that the high- st levels of Al-2 were produced by periodontal pathogens such as Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum {20}. In addition, Aggregatibacter actinomyeetemicomitans ‘was shown to possess a luxS gene and produce Al-2. The luxS gene from. actinomycetemcomitans, when expressed in Escherichia col, was able to complement a P. gingivalis luxS mutant by restoring the expression of two Al-2 responsive genes, uvrB and hasF, 10 ‘wild-type levels 21 |. This study demonstrated that P. gingivalisan tect the Al-2 signal from A, actinomycetemicomitans, and it pro= vided the first indication that interspecies communication using ‘Al-2 may occur in oral bioflims. Clearer evidence for Al-2-mediated interspecies communica- tion by P gingivalis came from coculture studies with streptococcus gordonii (22), These data indicate that S. gordonii and P. gingivalis sense Al-2 produced by either organism, and translate the signal {nto a biofilm phenotype. An important function for AI-2 in muta listic associations was demonstrated in studies of dual-species biofilms formed with Actinomyces oris and Streptococcus orl [23 ‘Metabolic cues: Streptococcal 202 is an important molecule {in competition with and communication between oral bacteria Op is secteted by Streptococcus viridans, including Streptococ- cus sanguin, S. oalis,Streptacoccus mits, . gordonii, Streptococcus parasanguinis and some strains of S. mutans, and it is responsi- ble for the greenish tinge (a-haemolysis) produced when these ‘organisms ate cultured on blood agar: In vitro, in closed batch cul ture, HO» can reach concentrations sufficient to kill various other oral bacteria. However, the mouth is an open system in which small molecules such as HO are continually washed away from the biofilm. At sublethal concentrations, HOz has been shown t0 induce a variety of responses in oral bacteria [24]. In S. viridans, S. sanguinis and S. gordonii, HO triggers the release of DNA by a ‘mechanism that does not involve cell ysis [25]. Extracellular DNAis an important component of bacterial biofilms. The release of DNA by streptococci may therefore help to stabilize the biofilm struc- ture, H:02 oxidizes macromolecules, and S. gordonii proteins are extensively oxidized during growth in aerobic batch culture. Some strains ofA ors produce catalase, which degrades H202 (25) '. viridans produces lactate, which is used as a substrate for energy production by A. actinomycetemcamirans and by Vellionelia ‘atypica, Interestingly, both of these organisms have been shown, to communicate with oral streptococci. In the case of . actino- -iycetemicomitans, sensing occu through detection of Ha02 [27]. A-actinomycetemcomitans produces a very restricted response to 205: just two genes were significantly upregulated by H0z in 4 microatray analysis. These were katA, encoding catalase, and pia. encoding a 33-kDa auter membrane protein that binds to the human serum protein factor H and provides resistance to serum ‘A Parashar cal /ora Sen nee ntormaional 12(2015) 37-42 a ‘Commensals Ve oO Pathogens a sea es ae CO OO Yo pellicle << Mutvalism and ——— commen: stage? Gtagestand 2) <— Transition bacterial growth Grage 3) ‘tledce 2 concetaton & stages wot a AE ce a SOOO Fig. 5. Relutlonsip between succession of orl communes and autoinducer 2: ln tis gure dental plaque developments shown with respect. tne. The selatve aout (of AL-2 production salsa shown by various cammensal and pathogen colonizers killing. One possibilty is that HO signals an increased likelihood of inflammation, and A actinomycetemcomitans benefits by prepar~ ing for the inflammatory onslaught (17) 4.1. Al-2 in spatiotemporal development of multispecies communities ‘The signalling molecule Al-2 has been praposed to act as a uni- versal intergeneric signalling molecule, and it has an important role in the formation of multispecies biofilms. When bacteria are brought together by co-aggregation, the effective AI2 threshold concentration can be reached when the praduction fate of AL-2 is lower than that necessary wien the bacteria are further apart. Ina model based on these principles, itis likely that different ‘concentrations of Al-2 play a part in the communication between, different species [28]. A schematic of this hypothesis that is rele- vant to bioftim development in the human oral cavity is presented inFig. 5 [4 The relative amount of Al-2 produced by commensal bacte- ria and pathogens is indicated. Commensals (depicted in stages 1 and 2) respond to the lowest AI-2 concentrations (below 100 pM), ‘which results in mutualism and bacterial growth, Initial coloniz~ fers such as streptococci (yellow) and Actinomyces (blue) bind to the salivary pellicle (stage 1), which coats the enamel, and sub- ‘sequently grow together with Veillonella (purple) as multispecies biofilm communities (stage 2). As the commensal bacterial biomass increases by cell division and by accretion, the AI-2 concentration increases, whici improves the communication among transition ‘bacterial species such as Fusobacterium (orange: stage 3). Finally, ‘when the Al-2 concentration isthe highest (stage 4), the pathogens (red) are favoured for growth and they join the developing biofilm communities, Tis model offers a simple way to conceptualize the {importance of distance in crucial communication in each multspecies west 2 production Scent stage Land the msximum 3 Sage 4 community producing Al-2 and each community responding opti- ‘mally fo a particular local concentration of the signal |29]. Bacteria respond to Al-2 by internalizing the molecule; therefore, retention ‘of community-generated AI-2 and internalization of AI-2 by the ‘members of the community is essential for biofilm development. 5. Future perspectives The diversity of signalling opportunities within microbial com- ‘munities and the significant role of these molecules in coordinating gene expression and promoting biofilm formation have provided the impetus to investigate the potential of inhibitory analogues to disrupt these networks, thereby providing mechanisms to control or influence the development of dental plaque. Further, Q5 research, should include the development of future therapy for oral infec- tions. The Al-2 and CSP system has attracted attention as a target for weakening bacterial virulence by interfering with cell-to-cell communication. A new class of specifically targeted antimicrobial peptides (STAMPS) has recently been reported for use in a unique strategy [30], The STAMP have a two-sided structure. The fst isa short homing sequence of CPS that can be as unique to a bacterium, as.a fingerprint and ensures that the STAMPS will find their tar- gel. The second is a non-specific antibacterial peptide that is linked chemically tothe homing sequenceand killsthe targeted bacterium, on delivery 6. Conclusions 6.1, ‘The Great Bacterial Reef communteation and development inoral biofis* Consider that the Great Barrier Reef is home to thousands of species of plants and animals with spatio-temporally predictable 2 ‘A Parashar ea, / nal Scene ternal 12 (2015) 37-42 fish communities on coral reefs, and compare this withthe fact that human oral bacteria develop spatio-temporally predictable dental plaque communities on enamel after each oral hygiene procedure. This reassembling oforal bacterial communities over atime interval ‘of only a few hours offers an opportunity to investigate the role of ‘communication in community architecture and composition. ‘As in a city, where vibrant communities are formed by the mix- ing of people from different cultural and ethnic backgrounds, oral bacteria in biofilms sense their microbial neighbours and build pro- ductive mixed-species consortia, Signalling between bacteria may have important implications for the virulence of oral pathogens. Therefore, when assessing the ability of oral bacteria to cause dis- ‘ease, it is essential to consider the community in its entirety rather ‘than relying solely on observations of individual components. The ‘ongoing development of high-throughput techriques such as DNA microarrays and massively parallel sequencing is already greatly ‘enhancing studies of gene expression in mixed-species commu- nities, It remains fo be seen whether these approaches will lead to new interventions that can change the course of oral microbial diseases. Conflict of interest ‘The authors declare that they have no coc of interest. Source of funding No institutional fund involvement exist for this stuy. References In} cozhlan A stime iy. ew cents 1906:15:32-6, DB] Losick Katze D. Why and how bactera communicte? Sci Am Nouraret 7 [a] Wail Kole 8 Biotin, cy of microbes Bacteriol 2000-182:2675-9, Fal Kolenbrande PE, Falmer I Perasamy 5

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