logo

SCIENCE CHINA Earth Sciences, Volume 62, Issue 4: 609-618(2019) https://doi.org/10.1007/s11430-018-9332-1

Recent progress on signalling molecules of coral-associated microorganisms

More info
  • ReceivedFeb 27, 2018
  • AcceptedJan 22, 2019
  • PublishedMar 4, 2019

Abstract

Coral reefs have high primary productivity and are one of the most important ecosystems in the ocean. However, the health and stability of coral reefs are constantly threatened by climate change and human activities. The coral holobiont is a complex symbiosis between the coral animal, zooxanthellae, and the associated community of microorganisms including bacteria, archaea, viruses, etc. Coral-associated microorganisms are found to be important for the maintenance of coral health, and they are proposed to contribute to the acclimatization and adaptation of reef-building corals under rapid climate change. The coral-microbe interaction mediated by chemical signalling molecules is an important driving force for shaping the microbial communities. Herein, we summarize our current knowledge of the chemical signalling molecules involved in the interaction of the coral holobiont. Specifically, the cooperation and competition among microbes mediated by N-acyl homoserine lactones (AHLs), the interrelationship between microbes and hosts mediated by dimethylsulfoniopropionate (DMSP) and nitric oxide (NO), and the response of corals and microorganisms to reactive oxygen species (ROS) under environmental stresses are highlighted in this review. We further discuss the potential of manipulating the coral microbiome using signalling molecules to restore and protect coral reefs.


Funded by

the National Key R & D Program of China(Grant,No.,2017YFC0506303)

the National Natural Science Foundation of China(Grant,Nos.,41706172,31625001,41376174)

the Hainan Provincial Key R & D Program(Grant,No.,ZDYF2018108)


Acknowledgment

This work was supported by the National Key R & D Program of China (Grant No. 2017YFC0506303), the National Natural Science Foundation of China (Grant Nos. 41706172, 31625001 & 41376174) and the Hainan Provincial Key R & D Program (Grant No. ZDYF2018108).


References

[1] Ainsworth T D, Krause L, Bridge T, Torda G, Raina J B, Zakrzewski M, Gates R D, Padilla-Gamiño J L, Spalding H L, Smith C, Woolsey E S, Bourne D G, Bongaerts P, Hoegh-Guldberg O, Leggat W. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J, 2015, 9: 2261-2274 CrossRef PubMed Google Scholar

[2] Arora D P, Hossain S, Xu Y, Boon E M. Nitric oxide regulation of bacterial biofilms. Biochemistry, 2015, 54: 3717-3728 CrossRef PubMed Google Scholar

[3] Baird A H, Bhagooli R, Ralph P J, Takahashi S. Coral bleaching: The role of the host. Trends Ecol Evol, 2009, 24: 16-20 CrossRef PubMed Google Scholar

[4] Baker-Austin C, Oliver J D. Vibrio vulnificus: New insights into a deadly opportunistic pathogen. Environ Microbiol, 2018, 20: 423-430 CrossRef PubMed Google Scholar

[5] Banin E, Vassilakos D, Orr E, Martinez R J, Rosenberg E. Superoxide dismutase is a virulence factor produced by the coral bleaching pathogen Vibrio shiloi. Curr Microbiol, 2003, 46: 418-422 CrossRef PubMed Google Scholar

[6] Bhedi C D, Prevatte C W, Lookadoo M S, Waikel P A, Gillevet P M, Sikaroodi M, Campagna S R, Richardson L L. Elevated temperature enhances short- to medium-chain acyl homoserine lactone production by black band disease-associated vibrios. Microbiol Ecol, 2017, 93: fix005 CrossRef PubMed Google Scholar

[7] Bouchard J N, Yamasaki H. Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: A possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol, 2008, 49: 641-652 CrossRef PubMed Google Scholar

[8] Bourne D G, Dennis P G, Uthicke S, Soo R M, Tyson G W, Webster N. Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J, 2013, 7: 1452-1458 CrossRef PubMed Google Scholar

[9] Bourne D G, Morrow K M, Webster N S. Insights into the coral microbiome: Underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol, 2016, 70: 317-340 CrossRef PubMed Google Scholar

[10] Cai L, Tian R M, Zhou G, Tong H, Wong Y H, Zhang W, Chui A P Y, Xie J Y, Qiu J W, Ang P O, Liu S, Huang H, Qian P Y. Exploring coral microbiome assemblages in the South China Sea. Sci Rep, 2018, 8: 2428 CrossRef PubMed ADS Google Scholar

[11] Ceh J, Kilburn M R, Cliff J B, Raina J B, van Keulen M, Bourne D G. Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates. Ecol Evol, 2013, 3: 2393-2400 CrossRef Google Scholar

[12] Certner R H, Vollmer S V. Evidence for autoinduction and quorum sensing in white band disease-causing microbes on Acropora cervicornis. Sci Rep, 2015, 5: 11134 CrossRef PubMed ADS Google Scholar

[13] Certner R H, Vollmer S V. Inhibiting bacterial quorum sensing arrests coral disease development and disease-associated microbes. Environ Microbiol, 2018, 20: 645-657 CrossRef PubMed Google Scholar

[14] Chandler J R, Heilmann S, Mittler J E, Greenberg E P. Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model. ISME J, 2012, 6: 2219-2228 CrossRef PubMed Google Scholar

[15] Chugani S, Greenberg E P. An evolving perspective on the Pseudomonas aeruginosa orphan quorum sensing regulator QscR. Front Cell Infect Microbiol, 2014, 4: 152 CrossRef Google Scholar

[16] Cohen L J, Esterhazy D, Kim S H, Lemetre C, Aguilar R R, Gordon E A, Pickard A J, Cross J R, Emiliano A B, Han S M, Chu J, Vila-Farres X, Kaplitt J, Rogoz A, Calle P Y, Hunter C, Bitok J K, Brady S F. Commensal bacteria make GPCR ligands that mimic human signalling molecules. Nature, 2017, 549: 48-53 CrossRef PubMed ADS Google Scholar

[17] Cude W N, 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. Google Scholar

[18] Curson A R J, Todd J D, Sullivan M J, Johnston A W B. Catabolism of dimethylsulphoniopropionate: Microorganisms, enzymes and genes. Nat Rev Microbiol, 2011, 9: 849-859 CrossRef PubMed Google Scholar

[19] Davidson S K, Koropatnick T A, Kossmehl R, Sycuro L, McFall-Ngai M J. NO means “yes” in the squid-vibrio symbiosis: Nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol, 2004, 6: 1139-1151 CrossRef PubMed Google Scholar

[20] DeLoney-Marino C R, Wolfe A J, Visick K L. Chemoattraction of Vibrio fischeri to serine, nucleosides, and N-acetylneuraminic acid, a component of squid light-organ mucus. Appl Environ Microbiol, 2003, 69: 7527-7530 CrossRef Google Scholar

[21] Downs C A, Fauth J E, Halas J C, Dustan P, Bemiss J, Woodley C M. Oxidative stress and seasonal coral bleaching. Free Radical Biol Med, 2002, 33: 533-543 CrossRef Google Scholar

[22] Evans K C, Benomar S, Camuy-Vélez L A, Nasseri E B, Wang X, Neuenswander B, Chandler J R. Quorum-sensing control of antibiotic resistance stabilizes cooperation in Chromobacterium violaceum. ISME J, 2018, 12: 1263-1272 CrossRef PubMed Google Scholar

[23] Furlong C E, Marsillach J, Jarvik G P, Costa L G. 2016. Paraoxonases-1, -2 and -3: What are their functions? Chem Biol Interact, 259: 51–62. Google Scholar

[24] Gardner S G, Raina J B, Ralph P J, Petrou K. Reactive oxygen species (ROS) and dimethylated sulphur compounds in coral explants under acute thermal stress. J Exp Biol, 2017, 220: 1787-1791 CrossRef PubMed Google Scholar

[25] Garren M, Son K, Raina J B, Rusconi R, Menolascina F, Shapiro O H, Tout J, Bourne D G, Seymour J R, Stocker R. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J, 2014, 8: 999-1007 CrossRef PubMed Google Scholar

[26] Garren M, Son K, Tout J, Seymour J R, Stocker R. Temperature-induced behavioral switches in a bacterial coral pathogen. ISME J, 2016, 10: 1363-1372 CrossRef PubMed Google Scholar

[27] Glasl B, Herndl G J, Frade P R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J, 2016, 10: 2280-2292 CrossRef PubMed Google Scholar

[28] Golberg K, Eltzov E, Shnit-Orland M, Marks R S, Kushmaro A. Characterization of quorum sensing signals in coral-associated bacteria. Microb Ecol, 2011, 61: 783-792 CrossRef PubMed Google Scholar

[29] Golberg K, Pavlov V, Marks R S, Kushmaro A. Coral-associated bacteria, quorum sensing disrupters, and the regulation of biofouling. Biofouling, 2013, 29: 669-682 CrossRef PubMed Google Scholar

[30] Grandclement C, Tannières M, Moréra S, Dessaux Y, Faure D. Quorum quenching: Role in nature and applied developments. FEMS Microbiol Rev, 2016, 40: 86-116 CrossRef PubMed Google Scholar

[31] Guo X, Zheng L, Zhou W, Cui Z, Han P, Tian L, Wang X. 2011. A case study on chemical defense based on quorum sensing: Antibacterial activity of sponge-associated bacterium Pseudoalteromonas sp. NJ6-3-1 induced by quorum sensing mechanisms. Ann Microbiol, 61: 247–255. Google Scholar

[32] Hawkins T D, Bradley B J, Davy S K. Nitric oxide mediates coral bleaching through an apoptotic-like cell death pathway: Evidence from a model sea anemone-dinoflagellate symbiosis. FASEB J, 2013, 27: 4790-4798 CrossRef PubMed Google Scholar

[33] Henares B M, Higgins K E, Boon E M. Discovery of a nitric oxide responsive quorum sensing circuit in Vibrio harveyi. ACS Chem Biol, 2012, 7: 1331-1336 CrossRef PubMed Google Scholar

[34] Hernandez-Agreda A, Gates R D, Ainsworth T D. Defining the core microbiome in corals’ microbial soup. Trends Microbiol, 2017, 25: 125-140 CrossRef PubMed Google Scholar

[35] Hernandez-Agreda A, Leggat W, Bongaerts P, Ainsworth T D. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. MBio, 2016, 7: e00560 CrossRef PubMed Google Scholar

[36] Hossain S, Boon E M. Discovery of a novel nitric oxide binding protein and Nitric-Oxide-Responsive signaling pathway in Pseudomonas aeruginosa. ACS Infect Dis, 2017, 3: 454-461 CrossRef PubMed Google Scholar

[37] Hossain S, Nisbett L M, Boon E M. Discovery of two bacterial nitric oxide-responsive proteins and their roles in bacterial biofilm regulation. Acc Chem Res, 2017, 50: 1633-1639 CrossRef PubMed Google Scholar

[38] Hou J, Xu T, Su D, Wu Y, Cheng L, Wang J, Zhou Z, Wang Y. RNA-seq reveals extensive transcriptional response to heat stress in the stony coral Galaxea fascicularis. Front Genet, 2018, 9: 37 CrossRef PubMed Google Scholar

[39] Hoyland-Kroghsbo N M, Maerkedahl R B, Svenningsen S L. A quorum-sensing-induced bacteriophage defense mechanism. MBio, 2013, 4: e00362 CrossRef PubMed Google Scholar

[40] Hudaiberdiev S, Choudhary K S, Vera Alvarez R, Gelencsér Z, Ligeti B, Lamba D, Pongor S. Census of solo LuxR genes in prokaryotic genomes. Front Cell Infect Microbiol, 2015, 5: 20 CrossRef Google Scholar

[41] Hughes T P, Barnes M L, Bellwood D R, Cinner J E, Cumming G S, Jackson J B C, Kleypas J, van de Leemput I A, Lough J M, Morrison T H, Palumbi S R, van Nes E H, Scheffer M. Coral reefs in the Anthropocene. Nature, 2017a, 546: 82-90 CrossRef PubMed ADS Google Scholar

[42] Hughes T P, Kerry J T, Álvarez-Noriega M, Álvarez-Romero J G, Anderson K D, Baird A H, Babcock R C, Beger M, Bellwood D R, Berkelmans R, Bridge T C, Butler I R, Byrne M, Cantin N E, Comeau S, Connolly S R, Cumming G S, Dalton S J, Diaz-Pulido G, Eakin C M, Figueira W F, Gilmour J P, Harrison H B, Heron S F, Hoey A S, Hobbs J P A, Hoogenboom M O, Kennedy E V, Kuo C Y, Lough J M, Lowe R J, Liu G, McCulloch M T, Malcolm H A, McWilliam M J, Pandolfi J M, Pears R J, Pratchett M S, Schoepf V, Simpson T, Skirving W J, Sommer B, Torda G, Wachenfeld D R, Willis B L, Wilson S K. Global warming and recurrent mass bleaching of corals. Nature, 2017b, 543: 373-377 CrossRef PubMed ADS Google Scholar

[43] Johnson W M, Kido Soule M C, Kujawinski E B. Evidence for quorum sensing and differential metabolite production by a marine bacterium in response to DMSP. ISME J, 2016, 10: 2304-2316 CrossRef PubMed Google Scholar

[44] Joint I, Tait K, Callow M E, Callow J A, Milton D, Williams P, Cámara M. Cell-to-cell communication across the prokaryote-eukaryote boundary. Science, 2002, 298: 1207 CrossRef PubMed Google Scholar

[45] Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, Küsel K, Rillig M C, Rivett D W, Salles J F, van der Heijden M G A, Youssef N H, Zhang X, Wei Z, Hol W H G. Where less may be more: How the rare biosphere pulls ecosystems strings. ISME J, 2017, 11: 853-862 CrossRef PubMed Google Scholar

[46] Kendall M M, Sperandio V. What a dinner party! Mechanisms and functions of interkingdom signaling in host-pathogen associations. MBio, 2016, 7: e01748 CrossRef PubMed Google Scholar

[47] Kimes N E, Grim C J, Johnson W R, Hasan N A, Tall B D, Kothary M H, Kiss H, Munk A C, Tapia R, Green L, Detter C, Bruce D C, Brettin T S, Colwell R R, Morris P J. Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J, 2011, 6: 835-846 CrossRef PubMed Google Scholar

[48] Kuang W, Li J, Zhang S, Long L. 2015. Diversity and distribution of Actinobacteria associated with reef coral Porites lutea. Front Microbiol, 6: 1094. Google Scholar

[49] Lesser M P. Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu Rev Physiol, 2006, 68: 253-278 CrossRef Google Scholar

[50] Li J, Azam F, Zhang S. Outer membrane vesicles containing signalling molecules and active hydrolytic enzymes released by a coral pathogen Vibrio shilonii AK1. Environ Microbiol, 2016, 18: 3850-3866 CrossRef PubMed Google Scholar

[51] Li J, Chen Q, Long L J, Dong J D, Yang J, Zhang S. Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons. Sci Rep, 2014, 4: 7320 CrossRef PubMed ADS Google Scholar

[52] Li J, Kuang W, Long L, Zhang S. Production of quorum-sensing signals by bacteria in the coral mucus layer. Coral Reefs, 2017, 36: 1235-1241 CrossRef ADS Google Scholar

[53] Liang J, Yu K, Wang Y, Huang X, Huang W, Qin Z, Pan Z, Yao Q, Wang W, Wu Z. Distinct bacterial communities associated with massive and branching scleractinian corals and potential linkages to coral susceptibility to thermal or cold stress. Front Microbiol, 2017, 8: 979 CrossRef PubMed Google Scholar

[54] Lin S, Cheng S, Song B, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang L, Wang Z, Liu X, Yu S, Zeng P, Hao H, Zou Q, Chen C, Li Y, Wang Y, Xu C, Meng S, Xu X, Wang J, Yang H, Campbell D A, Sturm N R, Dagenais-Bellefeuille S, Morse D. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science, 2015, 350: 691-694 CrossRef PubMed ADS Google Scholar

[55] Ma Z P, Song Y, Cai Z H, Lin Z J, Lin G H, Wang Y, Zhou J. Anti-quorum sensing activities of selected coral symbiotic bacterial extracts from the South China Sea. Front Cell Infect Microbiol, 2018, 8: 144 CrossRef PubMed Google Scholar

[56] Mandel M J, Schaefer A L, Brennan C A, Heath-Heckman E A C, Deloney-Marino C R, McFall-Ngai M J, Ruby E G. Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl Environ Microbiol, 2012, 78: 4620-4626 CrossRef PubMed Google Scholar

[57] McClean K H, 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 A B, Williams P. Quorum sensing and Chromobacterium violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology, 1997, 143: 3703-3711 CrossRef PubMed Google Scholar

[58] Morohoshi T, Kato M, Fukamachi K, Kato N, Ikeda T. N-Acylhomoserine lactone regulates violacein production in Chromobacterium violaceum type strain ATCC 12472. FEMS MicroBiol Lett, 2008, 279: 124-130 CrossRef PubMed Google Scholar

[59] Munn C B. 2015. The role of vibrios in diseases of corals. Microbiol Spectr, 3: VE-0006-2014. Google Scholar

[60] Neave M J, Rachmawati R, Xun L, Michell C T, Bourne D G, Apprill A, Voolstra C R. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J, 2017, 11: 186-200 CrossRef PubMed Google Scholar

[61] O’Toole R, Lundberg S, Fredriksson S A, Jansson A, Nilsson B, Wolf-Watz H. 1999. The chemotactic response of Vibrio anguillarum to fish intestinal mucus is mediated by a combination of multiple mucus components. J Bacteriol, 181: 4308–4317. Google Scholar

[62] Papenfort K, Bassler B L. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol, 2016, 14: 576-588 CrossRef PubMed Google Scholar

[63] Patel H K, Suárez-Moreno Z R, Degrassi G, Subramoni S, González J F, Venturi V. Bacterial LuxR solos have evolved to respond to different molecules including signals from plants. Front Plant Sci, 2013, 4: 447 CrossRef PubMed Google Scholar

[64] Pereira C S, de Regt A K, Brito P H, Miller S T, Xavier K B. Identification of functional LsrB-like autoinducer-2 receptors. J Bacteriol, 2009, 191: 6975-6987 CrossRef PubMed Google Scholar

[65] Plate L, Marletta M A. Nitric oxide-sensing H-NOX proteins govern bacterial communal behavior. Trends Biochem Sci, 2013, 38: 566-575 CrossRef PubMed Google Scholar

[66] Raina J B, Clode P L, Cheong S, Bougoure J, Kilburn M R, Reeder A, Forêt S, Stat M, Beltran V, Thomas-Hall P, Tapiolas D, Motti C M, Gong B, Pernice M, Marjo C E, Seymour J R, Willis B L, Bourne D G. Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria. Elife, 2017, 6: e23008 CrossRef PubMed Google Scholar

[67] Raina J B, Dinsdale E A, Willis B L, Bourne D G. 2010. Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol, 18: 101–108. Google Scholar

[68] Rajput A, Kumar Kumar M. Computational exploration of putative LuxR solos in archaea and their functional implications in quorum sensing. Front Microbiol, 2017, 8: 798 CrossRef Google Scholar

[69] Reaka-Kudla M L. 1997. The global biodiversity of coral reefs: A comparison with rainforests. Biodiversity II: Understanding and protecting our biological resources, 2: 551. Google Scholar

[70] 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: 154 CrossRef PubMed Google Scholar

[71] Ritchie A J, Whittall C, Lazenby J J, Chhabra S R, Pritchard D I, Cooley M A. The immunomodulatory Pseudomonas aeruginosa signalling molecule N-(3-oxododecanoyl)-l-homoserine lactone enters mammalian cells in an unregulated fashion. Immunol Cell Biol, 2007, 85: 596-602 CrossRef PubMed Google Scholar

[72] Rosenberg E, Zilber-Rosenberg I. 2013. The hologenome concept: Human, animal and plant microbiota. Berlin: Springer. 178. Google Scholar

[73] Seymour J R, Simó R, Ahmed T, Stocker R. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science, 2010, 329: 342-345 CrossRef PubMed ADS Google Scholar

[74] Shiner E K, Terentyev D, Bryan A, Sennoune S, Martinez-Zaguilan R, Li G, Gyorke S, Williams S C, Rumbaugh K P. Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling. Cell Microbiol, 2006, 8: 1601-1610 CrossRef PubMed Google Scholar

[75] Simo R, Grimalt J O, Albaiges J. Field sampling and analysis of volatile reduced sulphur compounds in air, water and wet sediments by cryogenic trapping and gas chromatography. J Chromatogr A, 1993, 655: 301-307 CrossRef Google Scholar

[76] Subramoni S, Florez Salcedo D V, Suarez-Moreno Z R. A bioinformatic survey of distribution, conservation, and probable functions of LuxR solo regulators in bacteria. Front Cell Infect Microbiol, 2015, 5: 16 CrossRef PubMed Google Scholar

[77] Tait K, Hutchison Z, Thompson F L, Munn C B. Quorum sensing signal production and inhibition by coral-associated vibrios. Environ Microbiol Rep, 2010, 2: 145-150 CrossRef PubMed Google Scholar

[78] Tang K, Su Y, Brackman G, Cui F, Zhang Y, Shi X, Coenye T, Zhang X H. MomL, a novel marine-derived N-acyl homoserine lactonase from Muricauda olearia. Appl Environ Microbiol, 2015, 81: 774-782 CrossRef PubMed Google Scholar

[79] Tello E, Castellanos L, Arévalo-Ferro C, Duque C. Disruption in quorum-sensing systems and bacterial biofilm inhibition by cembranoid diterpenes isolated from the Octocoral Eunicea knighti. J Nat Prod, 2012, 75: 1637-1642 CrossRef PubMed Google Scholar

[80] Tout J, Jeffries T C, Petrou K, Tyson G W, Webster N S, Garren M, Stocker R, Ralph P J, Seymour J R. Chemotaxis by natural populations of coral reef bacteria. ISME J, 2015, 9: 1764-1777 CrossRef PubMed Google Scholar

[81] Wagner-Döbler I, Thiel V, Eberl L, Allgaier M, Bodor A, Meyer S, Ebner S, Hennig A, Pukall R, Schulz S. Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine Alphaproteobacteria. ChemBioChem, 2005, 6: 2195-2206 CrossRef PubMed Google Scholar

[82] Wangpraseurt D, Pernice M, Guagliardo P, Kilburn M R, Clode P L, Polerecky L, Kühl M. Light microenvironment and single-cell gradients of carbon fixation in tissues of symbiont-bearing corals. ISME J, 2016, 10: 788-792 CrossRef PubMed Google Scholar

[83] Webster N S, Reusch T B H. Microbial contributions to the persistence of coral reefs. ISME J, 2017, 11: 2167-2174 CrossRef PubMed Google Scholar

[84] Welsh R M, Zaneveld J R, Rosales S M, Payet J P, Burkepile D E, Thurber R V. Bacterial predation in a marine host-associated microbiome. ISME J, 2016, 10: 1540-1544 CrossRef PubMed Google Scholar

[85] Wheeler G L, Tait K, Taylor A, Brownlee C, Joint I. Acyl-homoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant Cell Environ, 2006, 29: 608-618 CrossRef Google Scholar

[86] Winans S C. A new family of quorum sensing pheromones synthesized using S-adenosylmethionine and Acyl-CoAs. Mol Microbiol, 2011, 79: 1403-1406 CrossRef PubMed Google Scholar

[87] Yates E A, Philipp B, Buckley C, Atkinson S, Chhabra S R, Sockett R E, Goldner M, Dessaux Y, Camara M, Smith H, Williams P. N-Acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infection Immun, 2002, 70: 5635-5646 CrossRef Google Scholar

[88] Ye X, Zhu J, Wang H. 2017. Advances in quorum-sensing LuxR solos in bacteria. Acta Microbiol Sin, 57: 341–349. Google Scholar

[89] Zhang T, Diaz J M, Brighi C, Parsons R J, McNally S, Apprill A, Hansel C M. Dark production of extracellular superoxide by the coral Porites astreoides and representative symbionts. Front Mar Sci, 2016, 3: 232 CrossRef Google Scholar

[90] Zhang Y, Yang Q, Ling J, Van Nostrand J D, Shi Z, Zhou J, Dong J. 2016. The shifts of diazotrophic communities in spring and summer associated with coral Galaxea astreata, Pavona decussata, and Porites lutea. Front Microbiol, 7: 1870. Google Scholar

[91] Zhou G, Cai L, Yuan T, Tian R, Tong H, Zhang W, Jiang L, Guo M, Liu S, Qian P Y, Huang H. Microbiome dynamics in early life stages of the scleractinian coral Acropora gemmifera in response to elevated pCO2. Environ Microbiol, 2017, 19: 3342-3352 CrossRef PubMed Google Scholar

[92] Zhou J, Jin H, Cai Z H. 2014. A review of the role and function of microbes in coral reef ecosystem. Chin J Appl Ecol 25: 919–930. Google Scholar

[93] Ziegler M, Seneca F O, Yum L K, Palumbi S R, Voolstra C R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun, 2017, 8: 14213 CrossRef PubMed ADS Google Scholar

[94] Zimmer B L, May A L, Bhedi C D, Dearth S P, Prevatte C W, Pratte Z, Campagna S R, Richardson L L. Quorum sensing signal production and microbial interactions in a polymicrobial disease of corals and the coral surface mucopolysaccharide layer. PLoS ONE, 2014, 9: e108541 CrossRef PubMed ADS Google Scholar

  • Figure 1

    Signal transduction mediated by chemical signalling molecules in coral-microbe symbiosis. QS, DMSP, NO and ROS are important mediators in coral-microbial symbiosis. Increasing temperature can promote the production of DMSP, NO and ROS. NO can promote the diffusion of ROS, while DMSP has antioxidant activity. Meanwhile, the increase in temperature can promote the secretion of AHLs by vibrios and promote the chemotaxis of vibrios to DMSP. Moreover, vibrios can respond to host NO signals by the receptor protein H-NOX, and its downstream signalling pathway is integrated into the QS pathway to regulate the expression of related genes. These findings suggest that these chemical factors may be closely related, but their specific mechanisms need to be further studied.

  • Figure 2

    Classical AHL QS pathway and different AHL signalling molecules. (a) The classical LuxI/R QS pathway in Vibrio fischeri. The AHL signalling molecule, N-3-oxohexanoyl-L-homoserine lactone (3OC6-HSL), is synthesized by LuxI. The binding of 3OC6-HSL to LuxR activates the expression of downstream genes. (b) All AHLs have a lactone ring and show differences in the acyl chains.

Copyright 2020 Science China Press Co., Ltd. 《中国科学》杂志社有限责任公司 版权所有

京ICP备18024590号-1