Microbial communication, particularly that of quorum sensing, plays an important role in regulating gene expression in a range of organisms. Although this phenomenon has been well studied in relation to, for example, virulence gene regulation, the focus of this article is to review our understanding of the role of microbial communication in extreme environments. Cell signaling regulates many important microbial processes and may play a pivotal role in driving microbial functional diversity and ultimately ecosystem function in extreme environments. Several recent studies have characterized cell signaling in modern analogs to early Earth communities (microbial mats), and characterization of cell signaling systems in these communities may provide unique insights in understanding the microbial interactions involved in function and survival in extreme environments. Cell signaling is a fundamental process that may have co-evolved with communities and environmental conditions on the early Earth. Without cell signaling, evolutionary pressures may have even resulted in the extinction rather than evolution of certain microbial groups. One of the biggest challenges in extremophile biology is understanding how and why some microbial functional groups are located where logically they would not be expected to survive, and tightly regulated communication may be key. Finally, quorum sensing has been recently identified for the first time in archaea, and thus communication at multiple levels (potentially even inter-domain) may be fundamental in extreme environments.
References
[1]
Bassler, B. Small Talk: Cell-to-Cell Communication in Bacteria. Cell？2002, 109, 421–424, doi:10.1016/S0092-8674(02)00749-3.
[2]
Dobretsov, S.; Teplitski, M.; Paul, V. Mini-review: Quorum sensing in the marine environment and its relationship to biofouling. Biofouling？2012, 25, 413–427.
[3]
Fuqua, C.; Parsek, M.; Greenberg, P. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Ann. Rev. Gen.？2001, 35, 439–468, doi:10.1146/annurev.genet.35.102401.090913.
[4]
Rivas, M.; Seeger, M.; Holmes, D.; Jedlicki, E. A Lux-like quorum sensing system in the extreme acidophile Acidithiobacillus. ferrooxidans. Biol. Res.？2005, 38, 283–297.
[5]
Chaphalkar, A.; Salunkhe, N. Phylogenetic analysis of nitrogen-fixing and quorum sensing bacteria. Int. J. Bioinf. Res.？2010, 2, 17–32.
[6]
Fuqua, C.; Winans, S.; Greenberg, E. Census and consensus in bacterial ecosystems—the LuxR-LuxI family of quorum-sensing transcriptional regulators. Ann. Rev. Microbiol.？1996, 50, 727–751, doi:10.1146/annurev.micro.50.1.727.
[7]
Pituka, E.V.; Hoover, R.B. Microbial extremophiles at the limits of life. Crit. Rev. Microbiol.？2007, 33, 183–209, doi:10.1080/10408410701451948.
[8]
Van den Burg, B. Extremophiles as a source for novel enzymes. Curr. Opin. Microbiol.？2003, 6, 213–218, doi:10.1016/S1369-5274(03)00060-2.
[9]
Sharif, D.I.; Gallon, J.; Smith, C.J.; Dudley, E. Quorum sensing in cyanobacteria: N-octanoyl-homoserine lactone release and response, by the epilithic colonial cyanobacterium Gloeothece PCC6909. ISME J.？2008, 2, 1171–1182, doi:10.1038/ismej.2008.68.
[10]
Zhang, G.; Zhang, F.; Ding, G.; Li, J.; Guo, X.; Zhu, J.; Zhou, L.; Cai, S.; Liu, X.; Luo, Y.; et al. Acyl homoserine lactone-based quorum sensing in a methanogenic archaeon. ISME J.？2012, 6, 1–9, doi:10.1038/ismej.2011.71.
[11]
Miller, M.; Bassler, B. Quorum Sensing in Bacteria. Ann. Rev. Microbiol.？2001, 55, 165–199, doi:10.1146/annurev.micro.55.1.165.
[12]
Yates, E.A.; Philipp, B.; Buckley, C.; Atkinson, S.; Chhabra, S.; Sockett, R.E.; Goldner, M.; Dessaux, Y.; Camara, M.; Smith, H.; Williams, P.; et al. N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect. Immun.？2002, 70, 5635–5646, doi:10.1128/IAI.70.10.5635-5646.2002.
[13]
Decho, A.W.; Visscher, P.T.; Ferry, J.; Kawaguchi, T.; He, L.; Przekop, K.M.; Norman, R.S.; Reid, P. Autoinducers extracted from microbial mats reveal a surprising diversity of N-acylhomoserine lactones (AHLs) and abundance changes that may relate to diel pH. Environ. Microbiol.？2009, 11, 409–420, doi:10.1111/j.1462-2920.2008.01780.x.
[14]
Xavier, K.; Bassler, B. Interference with AI-2-mediated bacterial cell-cell communication. Nature？2005, 437, 750–753, doi:10.1038/nature03960.
[15]
Chen, X.; Schauder, S.; Potier, N.; Dorsselaer, A.V.; Pelczer, I.; Bassler, B.; Hughson, F. Structural identification of a bacterial quorum-sensing signal containing boron. Nature？2002, 5, 545–549.
[16]
Diggle, S.P.; Cornelis, P.; Williams, P.; Cámara, M. 4-quinolone signalling in Pseudomonas aeruginosa: Old molecules, new perspectives. IJMM？2006, 296, 83–91.
[17]
Johnson, M.; Montero, C.; Connors, S.; Shockley, K.; Bridger, S.; Kelly, R. Population density-dependent regulation of exopolysaccharide formation in the hyperthermophilic bacterium Thermotoga. maritima. Mol. Microbiol.？2005, 55, 664–674.
[18]
Smith, M.B.; Smith, J.N.; Swift, S.; Heffron, F.; Ahmer, B.M. SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J. Bacteriol.？2001, 183, 5733–5742, doi:10.1128/JB.183.19.5733-5742.2001.
[19]
Steindler, L.; Venturi, V. Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol. Lett.？2007, 266, 1–9, doi:10.1111/j.1574-6968.2006.00501.x.
[20]
Rajamani, S.; Zhu, J.; Pei, D.; Sayre, R. A LuxP-FRET-based reporter for the detection and quantification of AI-2 bacterial quorum-sensing signal compounds. Biochemistry？2007, 46, 3990–3997, doi:10.1021/bi602479e.
[21]
McClean, K.; Winson, M.K.; Fish, L.; Taylor, A.; Chhabra, S.R.; Camara, M.; Daykin, M.; Lamb, J.H.; Swift, S.; Bycroft, B.W.; Stewart, G.S.; Williams, P. Quorum sensing and Chromobacterium violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Mol. Microbiol.？1997, 143, 3703–3711.
[22]
Llamas, I.; Quesada, E.; Martínez-Cánovas, M.J.; Gronquist, M.; Eberhard, A.; González, J.E. Quorum sensing in halophilic bacteria: detection of N-acyl-homoserine lactones in the exopolysaccharide-producing species of Halomonas. Extremophiles？2005, 9, 333–341, doi:10.1007/s00792-005-0448-1.
[23]
Paggi, R.; Martone, C.; Fuqua, C.; de Castro, R. Detection of quorum sensing signals in the haloalkaliphilic archaeon Natronococcus. occultus. FEMS Microbiol. Lett.？2003, 221, 49–52, doi:10.1016/S0378-1097(03)00174-5.
[24]
Visscher, P.T.; Dupraz, C.; Braissant, O.; Gallagher, K.L.; Glunk, C.; Casillas, L.; Reed, R.E. Biogeochemistry of carbon cycling in hypersaline mats: Linking the present to the past through biosignatures. In Cellular Origin,Life in Extreme Habitats and Astrobiology :Microbial Mats; Seckbach, J., Oren, A., Eds.; Springer Verlag: Berlin, Germany, 2010; Volume 14, pp. 443–468.
[25]
Margesin, R.; Schinner, F. Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles.？2001, 5, 73–83, doi:10.1007/s007920100184.
[26]
Penesyan, R.; Madrid, E.; D'Alessandro, C.; Cerletti, M.; de Castro, R. Growth phase-dependent biosynthesis of Nep, a halolysin-like protease secreted by the alkaliphilic haloarchaean Natrialba. magadii. Lett. Appl. Microbiol.？2010, 51, 36–41.
[27]
Decho, A.W. Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Mar. Biol. Ann. Rev.？1990, 28, 73–153.
[28]
Decho, A.W. Microbial biofilms in intertidal systems: An overview. Continental Shelf Res.？2000, 20, 1257–1273, doi:10.1016/S0278-4343(00)00022-4.
[29]
Averhoff, B.; Muller, V. Exploring research frontiers in microbiology- recent advances in halophilic and thermophilic extremophiles. Res. Microbiol.？2010, 161, 506–514, doi:10.1016/j.resmic.2010.05.006.
[30]
Sewald, X.; Saum, S.; Palm, P.; Pfeiffer, F.; Oesterhelt, D.; Muller, V. Autoinducer-2-Producing Protein LuxS, a Novel Salt- and Chloride-Induced Protein in the moderately halophilic Bacterium Halobacillus. halophilus. Appl. Environ. Microbiol.？2007, 73, 371–379.
[31]
DasSarma, S.; DasSarma, P. Halophiles. In Encyclopedia of Life Sciences; Wiley: London, UK, 2006.
[32]
Natrah, F.; Kenmegne, M.; Wiyoto, W.; Sorgeloos, P.; Bossier, P.; Defoirdt, T. Effects of micro-algae commonly used in aquaculture on acyl-homoserine lactone quorum sensing. Aquaculture？2011, 317, 53–57, doi:10.1016/j.aquaculture.2011.04.038.
[33]
Calvo, C.; Martinez-Checa, F.; Mota, A.; Bejar, V.; Quesada, E. Quesada, E. Effects of cations, pH and sulfate on the viscosity and emulsifying activity of the Halomonas. eurihalina exopolysachharide. J. Ind. Microbiol. Biotechnol.？1998, 20, 205–209, doi:10.1038/sj.jim.2900513.
[34]
Bouchotroch, S.; Quesada, E.; del Moral, A.; Llamas, I.; Bejar, V. Halomonas. maura sp. nov., a novel moderately halophilic, exopolysachharide-producing bacterium. Int. J. Syst. Evol. Microbiol.？2001, 51, 1625–1632, doi:10.1099/00207713-51-5-1625.
[35]
Matinez-Canovas, M.; Quesada, E.; Llamas, I.; Bejar, V. Halomonas. ventosae sp. nov., a moderately halophilic, denitrifying, exopolysachharide-producing bacterium. Int. J. Syst. Evol. Microbiol.？2004, 54, 733–737, doi:10.1099/ijs.0.02942-0.
[36]
Martinez-Canovas, M.; Bejar, V.; Martinez-Checa, F.; Quesada, E. Halomonas. anticariensis sp. nov., from Fuente de Piedra, a saline-wetland wildfowl reserve in Malaga, southern Spain. Int. J. Syst. Evol. Microbiol.？2004, 54, 1329–1332, doi:10.1099/ijs.0.63108-0.
[37]
Baker-Austin, C.; Potrykus, J.; Wexler, M.; Bond, P.L.; Dopson, M. Biofilm development in the extremely acidophilic archaeon Ferroplasma. acidarmanus Fer1. Extremophiles？2010, 14, 485–491, doi:10.1007/s00792-010-0328-1.
[38]
Wenbin, N.; Dejuan, Z.; Feifan, L.; Lei, Y.; Peng, C.; Xiaoxuan, Y.; Hongyu, L. Quorum-sensing system in Acidithiobacillus. ferrooxidans involved in its resistance to Cu2+. Lett. Appl. Microbiol.？2011, 53, 84–91, doi:10.1111/j.1472-765X.2011.03066.x.
[39]
Penesyan, A.; Kjelleberg, S.; Egan, S. Development of novel drugs from marine surface associated microorganisms. Mar. Drugs？2010, 8, 438–459, doi:10.3390/md8030438.
[40]
Rivas, M.; Seeger, M.; Jedlicki, E.; Holmes, D. Second acyl homoserine lactone production system in the extreme acidophile Acidithiobacillus. ferrooxidans. Appl. Environ. Microbiol.？2007, 73, 3225–3231, doi:10.1128/AEM.02948-06.
[41]
Ruiz, L.; Valenzuela, S.; Castro, M.; Gonzalez, A.; Frezza, M.; Soulere, L.; Rohwerder, T.; Queneau, Y.; Doutheau, A.; Sand, W.; Jerez, C.; Guiliani, N. AHL communication is a widespread phenomenon in biomining bacteria and seems to be involved in mineral-adhesion efficiency. Hydrometallurgy？2008, 94, 133–137, doi:10.1016/j.hydromet.2008.05.028.
[42]
Moreno-Paz, M.; Gomez, M.; Arcas, A.; Parro, V. Environmental transcriptome analysis reveals physiological differences between biofilm and planktonic modes of life of the iron oxidising bacteria Leptospirillum. spp. in their natural microbial community. BMC Genomics？2010, 11, 404–418.
[43]
Hammer, B.; Bassler, B. Quorum sensing controls biofilm formation in Vibrio. cholera. Mol. Microbiol.？2003, 50, 101–114, doi:10.1046/j.1365-2958.2003.03688.x.
[44]
March, J.; Bentley, W. Quorum sensing and bacterial cross-talk in biotechnology. Curr. Opin. Biotechnol.？2004, 15, 495–502.
[45]
Rader, B.; Campagna, S.; Semmelhack, M.F.; Bassler, B.; Guillemin, K. The quorum-sensing molecule autoinducer 2 regulates motility and flagellar morphogenesis in Helicobacter pylori. J. Bacteriol.？2007, 189, 6109–6117, doi:10.1128/JB.00246-07.
[46]
Schopf, S.; Wanner, G.; Rachel, R.; Wirth, R. An archaeal bi-species biofilm formed by Pyrococcus. furiosus and Methanopyrus. kandleri. Arch. Microbiol.？2008, 190, 371–377, doi:10.1007/s00203-008-0371-9.
[47]
Nichols, J.; Johnson, M.; Chou, C.; Kelly, R. Temperature, not LuxS, mediates AI-2 formation in hydrothermal habitats. FEMS Microbiol. Ecol.？2009, 68, 173–181, doi:10.1111/j.1574-6941.2009.00662.x.
[48]
Medigue, C.; Krin, E.; Pascal, G.; Barbe, V.; Bernsel, A.; Bertin, P.; Cheung, F.; Cruveiller, S.; D'Amico, S.; Duillo, A.; et al. Coping with cold: The genome of the versatile marine Antarctica bacterium Pseudoalteromonas. haloplanktis TAC125. Genome Res.？2005, 15, 1325–1335, doi:10.1101/gr.4126905.
[49]
Riley, M.; Staley, J.; Danchin, A.; Wang, T.Z.; Brettin, T.S.; Hauser, L.J.; Land, M.L.; Thompson, L.S. Genomics of an extreme psychrophile, Psychromonas. ingrahamii. BMC Genomics？2008, 9, 1–19, doi:10.1186/1471-2164-9-1.
[50]
Rezzonico, F.; Duffy, B. Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol.？2008, 8, 1–19, doi:10.1186/1471-2180-8-1.
Bodor, A.; Elxnat, B.; Thiel, V.; Schulz, S.; Wagner-Dobler, I. Potential for luxS related signalling in marine bacteria of autoinducer-2 in the genus Shewanella. BMC Microbiol.？2008, 8, 1–9, doi:10.1186/1471-2180-8-1.
[53]
Tait, K.; Williamson, H.; Atkinson, S.; Williams, P.; Camara, M.; Joint, I. Turnover of quorum sensing signal molecules modulates cross-kingdom signaling. Environ. Microbiol.？2009, 11, 1792–1802, doi:10.1111/j.1462-2920.2009.01904.x.
[54]
Sun, J.; Daniel, R.; Wagner-Dobler, I.; Zeng, A. Is autoinducer-2 a universal signal for interspecies communication- a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol. Biol.？2004, 4, 1–11, doi:10.1186/1471-2148-4-1.
[55]
Yuan, M.; Chen, M.; Zhang, W.; Lu, W.; Wang, J.; Yang, M.; Zhao, P.; Tang, R.; Li, X.; Hao, Y.; et al. Genome sequence and transcriptome analysis of the radioresistant bacterium Deinococcus. gobiensis: Insights into the extreme environmental adaptations. PLos One.？2012, 7, 34458–34551.
[56]
Ng, F.S.W.; Wright, D.M.; Seah, S.Y.K. Characterization of a phosphotriesterase-like lactonase from Sulfolobus. solfataricus and its immobilization for disruption of quorum sensing. Appl. Environ. Microbiol.？2011, 77, 1181–1186, doi:10.1128/AEM.01642-10.
[57]
Holden, M.T.; Chhabra, S.R.; Nys, R.; Stead, P.; Bainton, N.; Hill, P.; Manefield, M.; Kumar, N.; Labatte, M.; England, D.; et al. Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol. Microbiol.？1999, 33, 1254–1266.
[58]
Tommonaro, G.; Abbamondi, G.R.; Iodice, C.; Tait, K.; de Rosa, S. Diketopiperazines produced by the halophilic archaeon, Haloterrigena hispanica, activate AHL bioreporters. Microb. Ecol.？2012, 63, 490–495, doi:10.1007/s00248-011-9980-y.
[59]
Braissant, O.; Decho, A.W.; Przekop, K.M.; Gallagher, K.L.; Glunk, C.; Dupraz, C.; Visscher, P.T. Characteristics and turnover of exopolymeric substances (EPS) in a hypersaline microbial mat. FEMS Microbiol. Ecol.？2009, 67, 293–307, doi:10.1111/j.1574-6941.2008.00614.x.
[60]
Decho, A.; Norman, S.; Visscher, P.T. Quorum sensing in natural environments: Emerging views from microbial mats. Trends Microbiol.？2010, 18, 73–80, doi:10.1016/j.tim.2009.12.008.
[61]
Visscher, P.T.; Prins, R.A.; van Gemerden, H. Rates of sulfate reduction and thiosulfate consumption in a marine microbial mat. FEMS Microbiol. Ecol.？1992, 86, 283–294, doi:10.1111/j.1574-6968.1992.tb04820.x.
[62]
Sharma, A.; Kawarabayasi, Y.; Satyanarayana, T. Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles.？2012, 16, 1–19, doi:10.1007/s00792-011-0402-3.
[63]
Abe, F.; Horikoshi, K. The biotechnological potential of piezophiles. Trends Biotechnol.？2001, 19, 102–108, doi:10.1016/S0167-7799(00)01539-0.
[64]
D'Alessandro, C.; de Castra, R.; Gimenez, M.; Paggi, R. Effect of nutritional conditions on extracellular protease production by the haloalkaliphilic archaeon Natrialba. magadii. Lett. Appl. Microbiol.？2007, 44, 637–642, doi:10.1111/j.1472-765X.2007.02122.x.
[65]
Kanai, H.; Kobayashi, T.; Aono, R.; Kudo, T. Natronococcus. amylolyticus sp. nov., a haloalkaliphilic archaeon. Int. J. Syst. Bacteriol.？1995, 45, 762–766, doi:10.1099/00207713-45-4-762.
[66]
Bai, A.; Rai, V. Bacterial Quorum Sensing and Food Industry. Comprehensive Rev. Food Sci. Food Saf.？2011, 10, 184–194.
[67]
Fleet, G. Yeast interactions and wine flavor. Int. J. Food Microbiol.？2003, 86, 11–22, doi:10.1016/S0168-1605(03)00245-9.
