Microorganisms are a repository of interesting metabolites and functions. Therefore, accessing them is an important exercise for advancing not only basic questions about their physiology but also to advance technological applications. In this sense, increasing the culturability of environmental microorganisms remains an important endeavor for modern microbiology. Because microorganisms do not live in isolation in their environments, molecules can be added to the cultivation strategies to "inform them" that they are present in growth-permissive environmental conditions. Signaling molecules such as acyl-homoserine lactones and 3',5'-cyclic adenosine monophosphate belong to the plethora of molecules used by bacteria to communicate with each other in a phenomenon called quorum sensing. Therefore, including quorum sensing molecules can be an incentive for microorganisms, specifically soil bacteria, to increase their numbers on solid media.

Department of Biochemistry and Microbiology University of Chemistry and Technology Faculty of Food and Biochemical Technology Prague Czech Republic

Department of Water Technology and Environmental Engineering University of Chemistry and Technology Prague Prague Czechia

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Pascoal F, Magalhães C, Costa R. 2020. The link between the ecology of the prokaryotic rare biosphere and its biotechnological potential. Front Microbiol 11:231. doi:10.3389/fmicb.2020.00231 PubMed DOI PMC

West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat Rev Microbiol 4:597–607. doi:10.1038/nrmicro1461 PubMed DOI

Schuster M, Sexton DJ, Diggle SP, Greenberg EP. 2013. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol 67:43–63. doi:10.1146/annurev-micro-092412-155635 PubMed DOI

Whitehead NA, Barnard AML, Slater H, Simpson NJL, Salmond GPC. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol Rev 25:365–404. doi:10.1111/j.1574-6976.2001.tb00583.x PubMed DOI

Almeida FA de, Pimentel-Filho N de J, Pinto UM, Mantovani HC, Oliveira LL de, Vanetti MCD. 2017. Acyl homoserine lactone-based quorum sensing stimulates biofilm formation by Salmonella Enteritidis in anaerobic conditions. Arch Microbiol 199:475–486. doi:10.1007/s00203-016-1313-6 PubMed DOI

Andersson RA, Eriksson ARB, Heikinheimo R, Mäe A, Pirhonen M, Kõiv V, Hyytiäinen H, Tuikkala A, Palva ET. 2000. Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expREcc. Mol Plant Microbe Interact 13:384–393. doi:10.1094/MPMI.2000.13.4.384 PubMed DOI

Bowden SD, Eyres A, Chung JCS, Monson RE, Thompson A, Salmond GPC, Spring DR, Welch M. 2013. Virulence in Pectobacterium atrosepticum is regulated by a coincidence circuit involving quorum sensing and the stress alarmone, (p)ppGpp.. Mol Microbiol 90:457–471. doi:10.1111/mmi.12369 PubMed DOI

Atkinson S, Chang C-Y, Sockett RE, Cámara M, Williams P. 2006. Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J Bacteriol 188:1451–1461. doi:10.1128/JB.188.4.1451-1461.2006 PubMed DOI PMC

Chong G, Kimyon O, Rice SA, Kjelleberg S, Manefield M. 2012. The presence and role of bacterial quorum sensing in activated sludge. Microb Biotechnol 5:621–633. doi:10.1111/j.1751-7915.2012.00348.x PubMed DOI PMC

Hassett DJ, Ma J-F, Elkins JG, McDermott TR, Ochsner UA, West SEH, Huang C-T, Fredericks J, Burnett S, Stewart PS, McFeters G, Passador L, Iglewski BH. 1999. Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34:1082–1093. doi:10.1046/j.1365-2958.1999.01672.x PubMed DOI

Botsford JL, Harman JG. 1992. Cyclic AMP in prokaryotes. Microbiol Rev 56:100–122. doi:10.1128/mr.56.1.100-122.1992 PubMed DOI PMC

Xu K, Lin L, Shen D, Chou S-H, Qian G. 2021. “Clp is a “busy” transcription factor in the bacterial warrior, Lysobacter enzymogenes” Comput Struct Biotechnol J 19:3564–3572. doi:10.1016/j.csbj.2021.06.020 PubMed DOI PMC

Bruns A, Cypionka H, Overmann J. 2002. Cyclic amp and acyl homoserine lactones increase the cultivation efficiency of heterotrophic bacteria from the central Baltic Sea. Appl Environ Microbiol 68:3978–3987. doi:10.1128/AEM.68.8.3978-3987.2002 PubMed DOI PMC

Bollmann A, Lewis K, Epstein SS. 2007. Incubation of environmental samples in a diffusion chamber increases the diversity of recovered isolates. Appl Environ Microbiol 73:6386–6390. doi:10.1128/AEM.01309-07 PubMed DOI PMC

Bruns A, Nübel U, Cypionka H, Overmann J. 2003. Effect of signal compounds and incubation conditions on the culturability of freshwater bacterioplankton. Appl Environ Microbiol 69:1980–1989. doi:10.1128/AEM.69.4.1980-1989.2003 PubMed DOI PMC

Rygaard AM, Thøgersen MS, Nielsen KF, Gram L, Bentzon-Tilia M. 2017. Effects of gelling agent and extracellular signaling molecules on the culturability of marine bacteria. Appl Environ Microbiol 83:e00243-17. doi:10.1128/AEM.00243-17 PubMed DOI PMC

Lopez Marin MA, Strejcek M, Junkova P, Suman J, Santrucek J, Uhlik O. 2021. Exploring the potential of Micrococcus luteus culture supernatant with resuscitation-promoting factor for enhancing the culturability of soil bacteria. Front Microbiol 12:685263. doi:10.3389/fmicb.2021.685263 PubMed DOI PMC

Fraraccio S, Strejcek M, Dolinova I, Macek T, Uhlik O. 2017. Secondary compound hypothesis revisited: selected plant secondary metabolites promote bacterial degradation of cis-1,2-dichloroethylene (cDCE). Sci Rep 7:8406. doi:10.1038/s41598-017-07760-1 PubMed DOI PMC

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. DADA2: high-resolution sample inference from illumina amplicon data. Nat Methods 13:581–583. doi:10.1038/nmeth.3869 PubMed DOI PMC

R Core Team . 2020. R: A language and environment for statistical computing, R foundation for statistical computing. , Vienna, Austria. Available from: https://www.R-project.org/

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–6. doi:10.1093/nar/gks1219 PubMed DOI PMC

McMurdie PJ, Holmes S. 2013. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. doi:10.1371/journal.pone.0061217 PubMed DOI PMC

Wright ES. 2016. Using DECIPHER v2. 0 to analyze big biological sequence data in R. The R Journal 8:352. doi:10.32614/RJ-2016-025 DOI

Li S, Chen K, Vähänissi V, Radevici I, Savin H, Oksanen J. 2022. Electron injection in metal assisted chemical etching as a fundamental mechanism for electroless electricity generation. J Phys Chem Lett 13:5648–5653. doi:10.1021/acs.jpclett.2c01302 PubMed DOI PMC

Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen T, Miller E, Bache S, Müller K, Ooms J, Robinson D, Seidel D, Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H. 2019. Welcome to the Tidyverse. JOSS 4:1686. doi:10.21105/joss.01686 DOI

Kassambara A. 2020. rstatix: Pipe-friendly framework for basic statistical tests. R package version 060.

Paulson JN, Stine OC, Bravo HC, Pop M. 2013. Differential abundance analysis for microbial marker-gene surveys. Nat Methods 10:1200–1202. doi:10.1038/nmeth.2658 PubMed DOI PMC

Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI. 2020. PICRUSt2 for prediction of Metagenome functions. Nat Biotechnol 38:685–688. doi:10.1038/s41587-020-0548-6 PubMed DOI PMC

Kanehisa M, Goto S. 2000. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. doi:10.1093/nar/28.1.27 PubMed DOI PMC

Wickham H. 2016. Ggplot2, . In Ggplot2: Elegant Graphics for data analysis. Springer-Verlag, Cham. doi:10.1007/978-3-319-24277-4 DOI

Rosselló-Móra R, Amann R. 2015. Past and future species definitions for bacteria and Archaea. Syst Appl Microbiol 38:209–216. doi:10.1016/j.syapm.2015.02.001 PubMed DOI

Zhou J, Zhang L, Qu J, Tian H, Li H. 2021. Culture-dependent and culture-independent analyses of the effects of signal compounds on microbial community dynamics in lake sediment. Environ Eng Sci 38:752–763. doi:10.1089/ees.2020.0246 DOI

Decho AW, Frey RL, Ferry JL. 2011. Chemical challenges to bacterial AHL signaling in the environment. Chem Rev 111:86–99. doi:10.1021/cr100311q PubMed DOI

Remuzgo-Martínez S, Lázaro-Díez M, Mayer C, Aranzamendi-Zaldumbide M, Padilla D, Calvo J, Marco F, Martínez-Martínez L, Icardo JM, Otero A, Ramos-Vivas J. 2015. Biofilm formation and quorum-sensing-molecule production by clinical isolates of Serratia liquefaciens. Appl Environ Microbiol 81:3306–3315. doi:10.1128/AEM.00088-15 PubMed DOI PMC

Jung BK, Khan AR, Hong S-J, Park G-S, Park Y-J, Kim H-J, Jeon H-J, Khan MA, Waqas M, Lee I-J, Lee S-E, Shin J-H. 2017. Quorum sensing activity of the plant growth-promoting rhizobacterium Serratia glossinae GS2 isolated from the sesame (Sesamum indicum L.) rhizosphere. Ann Microbiol 67:623–632. doi:10.1007/s13213-017-1291-1 DOI

Goh S-Y, Khan SA, Tee KK, Abu Kasim NH, Yin W-F, Chan K-G. 2016. Quorum sensing activity of Citrobacter amalonaticus L8A, a bacterium isolated from dental plaque. Sci Rep 6:20702. doi:10.1038/srep20702 PubMed DOI PMC

Romero M, Muras A, Mayer C, Buján N, Magariños B, Otero A. 2014. In vitro quenching of fish pathogen Edwardsiella tarda AHL production using marine bacterium Tenacibaculum sp. strain 20J cell extracts. Dis Aquat Organ 108:217–225. doi:10.3354/dao02697 PubMed DOI

Lithgow JK, Wilkinson A, Hardman A, Rodelas B, Wisniewski-Dyé F, Williams P, Downie JA. 2000. The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol Microbiol 37:81–97. doi:10.1046/j.1365-2958.2000.01960.x PubMed DOI

Priya K, Sulaiman J, How KY, Yin W-F, Chan K-G. 2018. Production of N-acyl homoserine lactones by Chromobacterium haemolyticum KM2 isolated from the river water in Malaysia. Arch Microbiol 200:1135–1142. doi:10.1007/s00203-018-1526-y PubMed DOI

Malott RJ, Baldwin A, Mahenthiralingam E, Sokol PA. 2005. Characterization of the cciIR Quorum-sensing system in Burkholderia cenocepacia. Infect Immun 73:4982–4992. doi:10.1128/IAI.73.8.4982-4992.2005 PubMed DOI PMC

Redfield RJ. 2002. Is Quorum sensing a side effect of diffusion sensing Trends Microbiol 10:365–370. doi:10.1016/s0966-842x(02)02400-9 PubMed DOI

Pribytkova T, Lightly TJ, Kumar B, Bernier SP, Sorensen JL, Surette MG, Cardona ST. 2014. The attenuated virulence of a Burkholderia cenocepacia paaABCDE mutant is due to inhibition of quorum sensing by release of phenylacetic acid. Mol Microbiol 94:522–536. doi:10.1111/mmi.12771 PubMed DOI

Sun Y, Guan Y, Zeng D, He K, Wu G. 2018. Metagenomics-based interpretation of AHLs-mediated quorum sensing in anammox biofilm reactors for low-strength wastewater treatment. Chem Eng J 344:42–52. doi:10.1016/j.cej.2018.03.047 DOI

Sun Y, Guan Y, Wang D, Liang K, Wu G. 2018. Potential roles of acyl homoserine lactone based quorum sensing in sequencing batch nitrifying biofilm reactors with or without the addition of organic carbon. Bioresource Technology 259:136–145. doi:10.1016/j.biortech.2018.03.025 PubMed DOI

Case RJ, Labbate M, Kjelleberg S. 2008. AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME J 2:345–349. doi:10.1038/ismej.2008.13 PubMed DOI

Kim A-L, Park S-Y, Lee C-H, Lee C-H, Lee J-K. 2014. Quorum quenching bacteria isolated from the sludge of a wastewater treatment plant and their application for controlling Biofilm formation. J Microbiol Biotechnol 24:1574–1582. doi:10.4014/jmb.1407.07009 PubMed DOI

Samanvitha K S, S SK, Samrot AV, P R, Paulraj P, P I, M C, Selvarani A J, Sruthi P D. 2019. Targeting acyl homoserine lactone (AHL) of Pseudomonas aeruginosa responsible for biofilm formation using plant metabolites. J Pure Appl Microbiol 13:1841–1846. doi:10.22207/JPAM.13.3.61 DOI

Yu Z, Chen J, Tan Y, Shen Y, Zhu L, Yu P. 2022. Phage predation promotes filamentous bacterium piscinibacter colonization and improves structural and hydraulic stability of microbial aggregates. Environ Sci Technol 56:16230–16239. doi:10.1021/acs.est.2c04745 PubMed DOI

Panchavinin S, Tobino T, Hara-Yamamura H, Matsuura N, Honda R. 2019. Candidates of quorum sensing bacteria in activated sludge associated with N-acyl homoserine lactones. Chemosphere 236:124292. doi:10.1016/j.chemosphere.2019.07.023 PubMed DOI

Kalam S, Basu A, Podile AR. 2022. Difficult-to-culture bacteria in the rhizosphere: the underexplored signature microbial groups. Pedosphere 32:75–89. doi:10.1016/S1002-0160(21)60062-0 DOI

Stevenson BS, Eichorst SA, Wertz JT, Schmidt TM, Breznak JA. 2004. New strategies for cultivation and detection of previously uncultured microbes. Appl Environ Microbiol 70:4748–4755. doi:10.1128/AEM.70.8.4748-4755.2004 PubMed DOI PMC

Bruns A, Hoffelner H, Overmann J. 2003. A novel approach for high throughput cultivation assays and the isolation of planktonic bacteria. FEMS Microbiol Ecol 45:161–171. doi:10.1016/S0168-6496(03)00133-8 PubMed DOI

Carneiro DG, Almeida FA, Aguilar AP, Vieira NM, Pinto UM, Mendes TAO, Vanetti MCD. 2020. Salmonella enterica optimizes metabolism after addition of acyl-homoserine lactone under anaerobic conditions. Front Microbiol 11:1459. doi:10.3389/fmicb.2020.01459 PubMed DOI PMC

Nichols D, Cahoon N, Trakhtenberg EM, Pham L, Mehta A, Belanger A, Kanigan T, Lewis K, Epstein SS. 2010. Use of ichip for high-throughput in situ cultivation of “uncultivable. Appl Environ Microbiol 76:2445–2450. doi:10.1128/AEM.01754-09 PubMed DOI PMC

Wang LL, Wu LJ, Li AJ, Hou BL, Jiang XM. 2018. Synergy of N-(3-oxohexanoyl)-L-homoserine lactone and tryptophan-like outer extracellular substances in granular sludge dominated by aerobic ammonia-oxidizing bacteria. Appl Microbiol Biotechnol 102:10779–10789. doi:10.1007/s00253-018-9437-z PubMed DOI

Zhu S, Wu H, Zhang C, Jie J, Liu Z, Zeng M, Wang C. 2018. Spoilage of refrigerated Litopenaeus vannamei: eavesdropping on Acinetobacter acyl-homoserine lactones promotes the spoilage potential of Shewanella baltica. J Food Sci Technol 55:1903–1912. doi:10.1007/s13197-018-3108-z PubMed DOI PMC

Liu F, Zhang Y, Liang H, Gao D. 2019. Specific quorum sensing molecules of ammonia oxidizers and their role during ammonium metabolism in Zhalong Wetland, China. Sci Total Environ 666:1106–1113. doi:10.1016/j.scitotenv.2019.02.261 PubMed DOI

Lumjiaktase P, Diggle SP, Loprasert S, Tungpradabkul S, Daykin M, Cámara M, Williams P, Kunakorn M. 2006. Quorum sensing regulates dpsA and the oxidative stress response in Burkholderia pseudomallei. Microbiology (Reading) 152:3651–3659. doi:10.1099/mic.0.29226-0 PubMed DOI