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First evidence of quorum sensing activity in bacteria associated with Antarctic sponges

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Abstract

Porifera dominate vast areas of the Antarctic shelves and are successfully colonized by bacteria. Quorum sensing (QS) is a cell-to-cell communication system based on bacterial population density that, enabling the coordination of group-based behaviour, plays a critical role in the successful colonization of higher organisms, also driving the formation of biofilm for adhesion to surfaces. In this study, the production of N-Acyl homoserine lactones (AHLs), signal molecules involved in the QS mechanism, was examined for 211 Antarctic sponge-associated Gram-negative bacteria. AHL production was screened by using three different AHL biodetection systems, i.e. Agrobacterium tumefaciens pZLR4, Chromobacterium violaceum CV026 and Pseudomonas putida pKR-C12 with optimal sensitivity to moderate-chain (C8–C12), short-chain (C4–C8) and long-chain (≥ C14) AHLs, respectively. 57.8% of tested isolates activated at least one of the monitor systems used and belonged mainly to bacterial genera that are known to be involved in surface colonization by biofilm production. A thin-layer chromatographic assay based on the A. tumefaciens reporter system was utilized to determine the AHL profiles of five selected positive isolates. Visible spots on thin-layer chromatography (TLC) plates were produced by Roseobacter sp. TB60 and Psychrobacter sp. TB67 (both from the sponge, Anoxycalyx joubini). The former probably produced N-(3-oxohexanoyl)-L-homoserine lactone (similar to the standard 3-oxo-C6-HSL), whereas the isolate TB67 produced molecules that were similar to the standard N-butanoyl-homoserine lactone (C4-HSL). The obtained results demonstrated that AHL-based signalling may play a key role in sponge–bacteria interactions also in the Antarctic environment.

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References

  • Bayer K, Kamke J, Hentschel U (2014) Quantification of bacterial and archaeal symbionts in high and low microbial abundance sponges using real-time PCR. FEMS Microbiol Ecol 89:679–690

    Article  PubMed  CAS  Google Scholar 

  • Brian-Jaisson F, Ortalo-Magné A, Guentas-Dombrowsky L, Armougom F, Blache Y (2014) identification of bacterial strains isolated from the Mediterranean Sea exhibiting different abilities of biofilm formation. Microb Ecol 68:94–110

    Article  PubMed  Google Scholar 

  • Chilton MD, Currier TC, Farrand SK, Bendich AJ, Gordon MP, Nester EW (1974) Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc Natl Acad Sci USA 71:3672–3676

    Article  PubMed  CAS  Google Scholar 

  • Cude WN, Buchan A (2013) Acyl-homoserine lactone-based quorum sensing in the Roseobacter clade: complex cell-to-cell communication controls multiple physiologies. Front Microbiol 4:336

    Article  PubMed  PubMed Central  Google Scholar 

  • Dang H, Li T, Chen M, Huang G (2008) Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Appl Environ Microbiol 74:52–60

    Article  PubMed  CAS  Google Scholar 

  • Doberva M, Sanchez-Ferandin S, Ferandin Y, Intertaglia L, Croué J, Suzuki M, Lebaron P, Lami R (2014) Genome sequence of the sponge-associated Ruegeria halocynthiae strain MOLA R1/13b, a marine Roseobacter with two quorum-sensing-based communication systems. Genome Announc 2(5):e00998

    PubMed  PubMed Central  Google Scholar 

  • Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fisheri luciferase. Biochemistry 20:2444–2453

    Article  PubMed  CAS  Google Scholar 

  • Farrand K, Qin Y, Oger P (2002) Quorum-sensing system of Agrobacterium plasmids: analysis and utility. Methods Enzymol 358:452–484

    Article  PubMed  CAS  Google Scholar 

  • Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468

    Article  PubMed  CAS  Google Scholar 

  • Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10:641–654

    Article  PubMed  CAS  Google Scholar 

  • Hughes DT, Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6:111–120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krick A, Kehraus S, Eberl L, Riedel K, Anke H, Kaesler I, Graeber I, Szewzyk U, Konig GM (2007) A marine Mesorhizobium sp. produces structurally novel long-chain N-Acyl-L- homoserine lactones. Appl Environ Microbiol 73:3587–3594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lavrov A, Kosevich IA (2016) Sponge cell reaggregation: cellular structure and morphogenetic potencies of multicellular aggregates. J Exp Zool A Ecol Genet Physiol 325:158–177

    Article  PubMed  Google Scholar 

  • Lerat E, Moran NA (2004) The evolutionary history of quorum-sensing systems in Bacteria. Mol Biol Evol 21:903–913

    Article  PubMed  CAS  Google Scholar 

  • Leys SP, Yahel G, Reidenbach MA, Tunnicliffe V, Shavit U, Reiswig HM (2011) The sponge pump: the role of current induced flow in the design of the sponge body plan. PLoS ONE 6:e27787

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lo Giudice A, Bruni V, Michaud L (2007) Characterization of Antarctic psychrotrophic bacteria with antibacterial activities against terrestrial microorganisms. J Basic Microbiol 47:496–505

    Article  PubMed  CAS  Google Scholar 

  • Maida I, Bosi E, Fondi M, Perrin E, Orlandini V, Papaleo MC, Mengoni A, de Pascale D, Tutino ML, Michaud L, Lo Giudice A, Fani R (2015) Antimicrobial activity of Pseudoalteromonas strains isolated from the Ross Sea (Antarctica) vs Cystic Fibrosis opportunistic pathogens. Hydrobiologia 761:443–457

    Article  CAS  Google Scholar 

  • Mangano S, Michaud L, Caruso C, Brilli M, Bruni V, Fani R, Lo Giudice A (2009) Antagonistic interactions among psychrotrophic cultivable bacteria isolated from Antarctic sponges: a preliminary analysis. Res Microbiol 160:27–37

    Article  PubMed  CAS  Google Scholar 

  • Mangano S, Michaud L, Caruso C, Lo Giudice A (2014) Metal and antibiotic-resistance in psychrotrophic bacteria associated with the Antarctic sponge Hemigellius pilosus (Kirkpatrick, 1907). Polar Biol 37:227–235

    Article  Google Scholar 

  • Martens T, Gram L, Grossart HP, Kessler D, Muller R, Meinhard S, Wenzel SC, Brinkhoff T (2007) Bacteria of the Roseobacter clade show potential for secondary metabolite production. Microb Ecol 54:31–42

    Article  PubMed  CAS  Google Scholar 

  • Martín-Rodríguez AJ, González-Orive A, Hernández-Creus A, Morales A, Dorta-Guerra R, Norte M, Martín VS, Fernández JJ (2014) On the influence of the culture conditions in bacterial antifouling bioassays and biofilm properties: Shewanella algae, a case study. BMC Microbiol 14:102

    Article  PubMed  PubMed Central  Google Scholar 

  • McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GSAB, Williams P (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703

    Article  PubMed  CAS  Google Scholar 

  • Michaud L, Di Cello F, Brilli M, Fani R, Lo Giudice A, Bruni V (2004) Biodiversity of cultivable psychrotrophic marine bacteria isolated from Terra Nova Bay (Ross Sea, Antarctica). FEMS Microbiol Lett 230:63–71

    Article  PubMed  CAS  Google Scholar 

  • Moghadam OS, Pourmand M, Aminharati F (2014) Biofilm formation and antimicrobial resistance in methicillin-resistant Staphylococcus aureus isolated from burn patients Iran. J Inf Develop Count 8:1511–1517

    Google Scholar 

  • Mohamed NM, Cicirelli EM, Kan J, Chen F, Fuqua C, Hill RT (2008) Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ Microbiol 10:75–86

    Article  PubMed  CAS  Google Scholar 

  • Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313–335

    PubMed  PubMed Central  CAS  Google Scholar 

  • Papaleo MC, Fondi M, Maida I, Perrin E, Lo Giudice A, Michaud L, Mangano S, Bartolucci G, Romoli R, Fani R (2012) Sponge-associated microbial Antarctic communities exhibiting antimicrobial activity against Burkholderia cepacia complex bacteria. Biotechnol Adv 30:272–293

    Article  PubMed  CAS  Google Scholar 

  • Papaleo MC, Romoli R, Bartolucci G, Maida I, Perrin E, Fondi M, Orlandini V, Mengoni A, Emiliani G, Tutino ML, Parrilli E, de Pascale D, Michaud L, Lo Giudice A, Fani R (2013) Bioactive volatile organic compounds from Antarctic (sponges) bacteria. New Biotechnol 30:824–838

    Article  CAS  Google Scholar 

  • Parsek MR, Greenberg EP (2000) Acyl-homoserine lactone quorum sensing in Gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. PNAS 97:8789–8793

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Rodríguez I, Bolognini M, Ricci J, Bini E, Vetriani C (2015) From deep-sea volcanoes to human pathogens: a conserved quorum-sensing signal in Epsilonproteo bacteria. ISME J 9:1222–1234

    Article  PubMed  Google Scholar 

  • Ravn L, Christensen AB, Molin S, Givskov M, Gram L (2001) Methods for identifying and quantifying acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J Microbiol Methods 44:239–251

    Article  PubMed  CAS  Google Scholar 

  • Riedel K, Hentzer M, Geisenberger O, Huber B, Steidle A, Wu H, Hoiby N, Givskov M, Molin S, Eberl L (2001) N-acylhomoserine lactone mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 47:3249–3262

    Article  Google Scholar 

  • Romero M, Avendano-Herrera R, Magarinos B, Camara M, Otero A (2010) Acylhomoserine lactone production and degradation by the fish pathogen Tenacibaculum maritimum, a member of the Cytophaga-Flavobacterium-Bacteroides (CFB) group. FEMS Microbiol Lett 304:131–139

    Article  PubMed  CAS  Google Scholar 

  • Ruby EG (1996) Lessons from a cooperative, bacterial-animal association: the Vibrio fisheri-Euprymna scolopes light organ symbiosis. Annu Rev Microbiol 50:591–624

    Article  PubMed  CAS  Google Scholar 

  • Saurav K, Burgsdorf I, Teta R, Esposito G, Bar-Shalom R, Costantino V, Steindler L (2016) Isolation of marine Paracoccus sp. Ss63 from the sponge Sarcotragus sp. and characterization of its quorum-sensing chemical-signaling molecules by LC-MS/MS analysis. Isr J Chem 56:330–340

    Article  CAS  Google Scholar 

  • Saurav K, Costantino V, Venturi V, Steindler L (2017) Quorum sensing inhibitors from the sea discovered using N-acyl-homoserine lactone-based biosensors. Mar Drugs 15:53

    Article  PubMed Central  CAS  Google Scholar 

  • Steindler L, Venturi V (2007) Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol Lett 266:1–9

    Article  PubMed  CAS  Google Scholar 

  • Taylor MW, Schupp PJ, Baille HJ, Charlton TS, de Nys R, Kjelleberg S, Steinberg PD (2004) Evidence for acyl homoserine lactone signal production in bacteria associated with marine sponges. Appl Environ Microbiol 70:4387–4389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vacelet J (1975) Etude en microscopie electronique de l’association entre bacteries et spongiaires du genre Verongia (Dictyoceratida). J Microsc Biol Cell 23:271–288

    Google Scholar 

  • Wagner-Dobler I, Thiel V, Eberl L, Allgaier M, Bodor A, Meyer S, Ebner S, Henning A, Pukall R, Schulz S (2005) Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine Alphaproteobacteria. Chem Bio Chem 6:2195–2206

    Article  PubMed  CAS  Google Scholar 

  • Webster NS, Negri AP, Munro MM, Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6:288–300

    Article  PubMed  Google Scholar 

  • Zan J, Fricke WF, Fuqua C, Ravel J, Hill RT (2011) Genome sequence of Ruegeria sp. strain KLH11, an N-acylhomoserine lactone-producing bacterium isolated from the marine sponge Mycale laxissima. J Bacteriol 193:5011–5012

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zeng Z, Cai X, Wang P, Guo Y, Liu X, Li B, Wang X (2017) Biofilm formation and heat stress induce pyomelanin production in deep-sea Pseudoalteromonas sp SM9913. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01822

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors wish to thank Vittorio Venturi and Laura Steindler (International Centre for Genetic Engineering, Trieste (Italy) for kindly providing the biomonitor systems used in this study, and for their professional support to S. Mangano during her stay in Trieste. We are very grateful also to three anonymous reviewers for their valuable comments and suggestions to improve the manuscript. The authors also thank Mrs Trays Ricciardi who edited the manuscript for improving English language. This work was supported by grants from the PNRA (Programma Nazionale di Ricerche in Antartide), the Italian Ministry of Education and Research (PEA 2004, Research Projects PNRA 2004/1.6 and PNRA16_00020) and the MNA (Museo Nazionale dell’Antartide).

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Authors and Affiliations

  1. Department of Chemical Biological, Pharmaceutical and Environmental Sciences, University of Messina, Viale F. Stagno d’Alcontres 31, 98166, Messina, Italy

    S. Mangano, C. Caruso, L. Michaud & A. Lo Giudice

  2. Institute for the Marine Coastal Environment, National Research Council (IAMC-CNR), Spianata San Raineri 86, 98122, Messina, Italy

    A. Lo Giudice

  3. Italian National Antarctic Museum (MNA, Associated Section of Messina - CIBAN), Messina, Italy

    A. Lo Giudice

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  1. S. Mangano
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Correspondence to A. Lo Giudice.

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Dedication: To the memory of our beloved Prof. Vivia Bruni.

Michaud L.—Posthumous.

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Mangano, S., Caruso, C., Michaud, L. et al. First evidence of quorum sensing activity in bacteria associated with Antarctic sponges. Polar Biol 41, 1435–1445 (2018). https://doi.org/10.1007/s00300-018-2296-3

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  • DOI: https://doi.org/10.1007/s00300-018-2296-3

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