Coral mucus rapidly induces chemokinesis and genome-wide transcriptional shifts toward early pathogenesis in a bacterial coral pathogen.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
16
12
2020
accepted:
25
05
2021
revised:
12
05
2021
pubmed:
26
6
2021
medline:
15
12
2021
entrez:
25
6
2021
Statut:
ppublish
Résumé
Elevated seawater temperatures have contributed to the rise of coral disease mediated by bacterial pathogens, such as the globally distributed Vibrio coralliilyticus, which utilizes coral mucus as a chemical cue to locate stressed corals. However, the physiological events in the pathogens that follow their entry into the coral host environment remain unknown. Here, we present simultaneous measurements of the behavioral and transcriptional responses of V. coralliilyticus BAA-450 incubated in coral mucus. Video microscopy revealed a strong and rapid chemokinetic behavioral response by the pathogen, characterized by a two-fold increase in average swimming speed within 6 min of coral mucus exposure. RNA sequencing showed that this bacterial behavior was accompanied by an equally rapid differential expression of 53% of the genes in the V. coralliilyticus genome. Specifically, transcript abundance 10 min after mucus exposure showed upregulation of genes involved in quorum sensing, biofilm formation, and nutrient metabolism, and downregulation of flagella synthesis and chemotaxis genes. After 60 min, we observed upregulation of genes associated with virulence, including zinc metalloproteases responsible for causing coral tissue damage and algal symbiont photoinactivation, and secretion systems that may export toxins. Together, our results suggest that V. coralliilyticus employs a suite of behavioral and transcriptional responses to rapidly shift into a distinct infection mode within minutes of exposure to the coral microenvironment.
Identifiants
pubmed: 34168314
doi: 10.1038/s41396-021-01024-7
pii: 10.1038/s41396-021-01024-7
pmc: PMC8630044
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3668-3682Informations de copyright
© 2021. The Author(s).
Références
De’Ath G, Fabricius KE, Sweatman H, Puotinen M. The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci U.S.A. 2012;109:17995–9.
pubmed: 23027961
pmcid: 3497744
doi: 10.1073/pnas.1208909109
Randall CJ, van Woesik R. Contemporary white-band disease in Caribbean corals driven by climate change. Nat Clim Chang. 2015;5:375–9.
doi: 10.1038/nclimate2530
Maynard J, van Hooidonk R, Eakin CM, Puotinen M, Garren M, Williams G, et al. Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nat Clim Chang. 2015;5:688–95.
doi: 10.1038/nclimate2625
Cziesielski MJ, Schmidt-Roach S, Aranda M. The past, present, and future of coral heat stress studies. Ecol Evol. 2019;9:10055–66.
pubmed: 31534713
pmcid: 6745681
doi: 10.1002/ece3.5576
Bourne D, Iida Y, Uthicke S, Smith-Keune C. Changes in coral-associated microbial communities during a bleaching event. ISME J. 2008;2:350–63.
pubmed: 18059490
doi: 10.1038/ismej.2007.112
van de Water JAJM, Chaib De Mares M, Dixon GB, Raina JB, Willis BL, Bourne DG, et al. Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef-building coral. Mol Ecol. 2018;27:1065–80.
pubmed: 29334418
doi: 10.1111/mec.14489
Sussman M, Mieog JC, Doyle J, Victor S, Willis BL, Bourne DG. Vibrio zinc-metalloprotease causes photoinactivation of coral endosymbionts and coral tissue lesions. PLoS ONE. 2009;4:1–14.
Ben-Haim Y, Zicherman-Keren M, Rosenberg E. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol. 2003;69:4236–41.
pubmed: 12839805
pmcid: 165124
doi: 10.1128/AEM.69.7.4236-4242.2003
Garren M, Son K, Raina J-B, Rusconi R, Menolascina F, Shapiro OH, et al. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J. 2014;8:999–1007.
pubmed: 24335830
doi: 10.1038/ismej.2013.210
Garren M, Son K, Tout J, Seymour JR, Stocker R. Temperature-induced behavioral switches in a bacterial coral pathogen. ISME J. 2016;10:1363–72.
pubmed: 26636553
doi: 10.1038/ismej.2015.216
Barbara GM, Mitchell JG. Marine bacterial organisation around point-like sources of amino acids. FEMS Microbiol Ecol. 2003;43:99–109.
pubmed: 19719700
doi: 10.1111/j.1574-6941.2003.tb01049.x
Seymour JR, Marcos, Stocker R. Resource patch formation and exploitation throughout the marine microbial food web. Am Nat. 2009;173:E15–29.
pubmed: 19053839
doi: 10.1086/593004
Son K, Menolascina F, Stocker R. Speed-dependent chemotactic precision in marine bacteria. Proc Natl Acad Sci U.S.A. 2016;113:8624–9.
pubmed: 27439872
pmcid: 4978249
doi: 10.1073/pnas.1602307113
Meron D, Efrony R, Johnson WR, Schaefer AL, Morris PJ, Rosenberg E, et al. Role of Flagella in virulence of the coral pathogen Vibrio coralliilyticus. Appl Environ Microbiol. 2009;75:5704–7.
pubmed: 19592536
pmcid: 2737915
doi: 10.1128/AEM.00198-09
Ushijima B, Häse CC. Influence of chemotaxis and swimming patterns on the virulence of the coral pathogen Vibrio coralliilyticus. J Bacteriol. 2018;200:1–16.
doi: 10.1128/JB.00791-17
Crossland CJ, Barnes DJ, Borowitzka MA. Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar Biol. 1980;60:81–90.
Davies PS. The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs. 1984;2:181–6.
Rix L, de Goeij JM, Mueller CE, Struck U, Middelburg JJ, van Duyl FC, et al. Coral mucus fuels the sponge loop in warm-and cold-water coral reef ecosystems. Sci Rep. 2016;6:1–11.
doi: 10.1038/srep18715
Naumann MS, Haas A, Struck U, Mayr C, El-Zibdah M, Wild C. Organic matter release by dominant hermatypic corals of the Northern Red Sea. Coral Reefs. 2010;29:649–59.
doi: 10.1007/s00338-010-0612-7
Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jørgensen BB. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature. 2004;428:66–70.
pubmed: 14999280
doi: 10.1038/nature02344
Bythell JC, Wild C. Biology and ecology of coral mucus release. J Exp Mar Bio Ecol. 2011;408:88–93.
doi: 10.1016/j.jembe.2011.07.028
Bakshani CR, Morales-Garcia AL, Althaus M, Wilcox MD, Pearson JP, Bythell JC, et al. Evolutionary conservation of the antimicrobial function of mucus: a first defence against infection. NPJ Biofilms Microbiomes. 2018;14:1–12.
Gibbin E, Gavish A, Krueger T, Kramarsky-Winter E, Shapiro O, Guiet R, et al. Vibrio coralliilyticus infection triggers a behavioural response and perturbs nutritional exchange and tissue integrity in a symbiotic coral. ISME J. 2019;13:989–1003.
Gavish AR, Shapiro OH, Kramarsky-Winter E, Vardi A. Microscale tracking of coral-vibrio interactions. ISME Communications. 2021;1:1–18.
Shapiro OH, Fernandez VI, Garren M, Guasto JS, Debaillon-Vesque FP, Kramarsky-Winter E, et al. Vortical ciliary flows actively enhance mass transport in reef corals. Proc Natl Acad Sci U.S.A. 2014;111:13391–6.
pubmed: 25192936
pmcid: 4169935
doi: 10.1073/pnas.1323094111
Seymour JR, Ahmed T, Stocker R. A microfluidic chemotaxis assay to study microbial behavior in diffusing nutrient patches. Limnol Oceanogr Methods. 2008;6:477–88.
doi: 10.4319/lom.2008.6.477
Penn K, Wang J, Fernando SC, Thompson JR. Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom. ISME J. 2014;8:1866–78.
pubmed: 24646695
pmcid: 4139720
doi: 10.1038/ismej.2014.27
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:1–21.
doi: 10.1186/s13059-014-0550-8
Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:1–12.
Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U.S.A. 2005;102:15545–50.
pubmed: 16199517
pmcid: 1239896
doi: 10.1073/pnas.0506580102
Mootha VK, Lindgren CM, Eriksson K-F, Subramanian A, Sihag S, Lehar J, et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003;34:267–73.
pubmed: 12808457
doi: 10.1038/ng1180
Schneider WR, Doetsch RN. Effect of viscosity on bacterial motility. J Bacteriol. 1974;117:696–701.
pubmed: 4204439
pmcid: 285562
doi: 10.1128/jb.117.2.696-701.1974
Martinez VA, Schwarz-Linek J, Reufer M, Wilson LG, Morozov AN, Poon WCK. Flagellated bacterial motility in polymer solutions. Proc Natl Acad Sci U.S.A. 2014;111:17771–6.
pubmed: 25468981
pmcid: 4273371
doi: 10.1073/pnas.1415460111
Kimes NE, Grim CJ, Johnson WR, Hasan NA, Tall BD, Kothary MH, et al. Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J. 2012;6:835–46.
pubmed: 22158392
doi: 10.1038/ismej.2011.154
Kojima S, Yamamoto K, Kawagishi I, Homma M. The polar flagellar motor of Vibrio cholerae is driven by an Na
pubmed: 10074090
pmcid: 93596
doi: 10.1128/JB.181.6.1927-1930.1999
Sowa Y, Hotta H, Homma M, Ishijima A. Torque-speed relationship of the Na
pubmed: 12662929
doi: 10.1016/S0022-2836(03)00176-1
Milo R, Phillips R. Cell biology by the numbers. 1st ed. New York, NY: Garland Science; 2016.
Crossland CJ. In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs. 1987;6:35–42.
doi: 10.1007/BF00302210
Wild C, Woyt H, Huettel M. Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser. 2005;287:87–98.
Ducklow HW, Mitchell R. Composition of mucus released by coral reef coelenterates. Limnol Oceanogr. 1979;24:706–14.
doi: 10.4319/lo.1979.24.4.0706
Meikle P, Richards GN, Yellowlees D. Structural determination of the oligosaccharide side chains from a glycoprotein isolated from the mucus of the coral Acropora formosa. J Biol Chem. 1987;262:16941–7.
pubmed: 2890643
doi: 10.1016/S0021-9258(18)45474-9
Coddeville B, Maes E, Ferrier-Pagès C, Guerardel Y. Glycan profiling of gel forming mucus layer from the scleractinian symbiotic coral Oculina arbuscula. Biomacromolecules. 2011;12:2064–73.
pubmed: 21517058
doi: 10.1021/bm101557v
Hasegawa H, Häse CC. TetR-type transcriptional regulator VtpR functions as a global regulator in Vibrio tubiashii. Appl Environ Microbiol. 2009;75:7602–9.
pubmed: 19837838
pmcid: 2794119
doi: 10.1128/AEM.01016-09
Ball AS, Chaparian RR, van Kessel JC. Quorum sensing gene regulation by LuxR/HapR master regulators in Vibrios. J Bacteriol. 2017;199:1–13.
Rutherford ST, Van Kessel JC, Shao Y, Bassler BL. AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev. 2011;25:397–408.
pubmed: 21325136
pmcid: 3042162
doi: 10.1101/gad.2015011
Hammer BK, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol. 2003;50:101–4.
pubmed: 14507367
doi: 10.1046/j.1365-2958.2003.03688.x
Waters CM, Lu W, Rabinowitz JD, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic Di-GMP levels and repression of vpsT. J Bacteriol. 2008;190:2527–36.
pubmed: 18223081
pmcid: 2293178
doi: 10.1128/JB.01756-07
Burger AH. Quorum Sensing in the Hawai’ian Coral Pathogen Vibrio coralliilyticus strain OCN008. University of Hawaii at Manoa; 2017.
Yildiz FH, Schoolnik GK. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci U.S.A. 1999;96:4028–33.
pubmed: 10097157
pmcid: 22414
doi: 10.1073/pnas.96.7.4028
Fong JCN, Syed KA, Klose KE, Yildiz FH. Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology. 2010;156:2757–69.
pubmed: 20466768
pmcid: 3068689
doi: 10.1099/mic.0.040196-0
Fong JCN, Karplus K, Schoolnik GK, Yildiz FH. Identification and characterization of RbmA, a novel protein required for the development of rugose colony morphology and biofilm structure in Vibrio cholerae. J Bacteriol. 2006;188:1049–59.
pubmed: 16428409
pmcid: 1347326
doi: 10.1128/JB.188.3.1049-1059.2006
Fong JCN, Yildiz FH. The rbmBCDEF gene cluster modulates development of rugose colony morphology and biofilm formation in Vibrio cholerae. J Bacteriol. 2007;189:2319–30.
pubmed: 17220218
pmcid: 1899372
doi: 10.1128/JB.01569-06
DiRita VJ, Mekalanos JJ. Periplasmic interaction between two membrane regulatory proteins, ToxR and ToxS, results in signal transduction and transcriptional activation. Cell. 1991;64:29–37.
pubmed: 1898871
doi: 10.1016/0092-8674(91)90206-E
Almagro-Moreno S, Root MZ, Taylor RK. Role of ToxS in the proteolytic cascade of virulence regulator ToxR in Vibrio cholerae. Mol Microbiol. 2015;98:963–76.
pubmed: 26316386
doi: 10.1111/mmi.13170
Lee SE, Ryu PY, Kim SY, Kim YR, Koh JT, Kim OJ, et al. Production of Vibrio vulnificus hemolysin in vivo and its pathogenic significance. Biochem Biophys Res Commun. 2004;324:86–91.
Senoh M, Okita Y, Shinoda S, Miyoshi S. The crucial amino acid residue related to inactivation of Vibrio vulnificus hemolysin. Micro Pathog. 2008;44:78–83.
doi: 10.1016/j.micpath.2007.07.002
Bröms JE, Ishikawa T, Wai SN, Sjöstedt A. A functional VipA-VipB interaction is required for the type VI secretion system activity of Vibrio cholerae O1 strain A1552. BMC Microbiol. 2013;13:1–12.
doi: 10.1186/1471-2180-13-96
Vizcaino MI, Johnson WR, Kimes NE, Williams K, Torralba M, Nelson KE, et al. Antimicrobial resistance of the coral pathogen Vibrio coralliilyticus and Caribbean sister phylotypes isolated from a diseased octocoral. Micro Ecol. 2010;59:646–57.
doi: 10.1007/s00248-010-9644-3
Ritchie KB. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser. 2006;322:1–14.
doi: 10.3354/meps322001
Nissimov J, Rosenberg E, Munn CB. Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett. 2009;292:210–5.
pubmed: 19191871
doi: 10.1111/j.1574-6968.2009.01490.x
Shnit-Orland M, Kushmaro A. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol. 2009;67:371–80.
pubmed: 19161430
doi: 10.1111/j.1574-6941.2008.00644.x
Rypien KL, Ward JR, Azam F. Antagonistic interactions among coral-associated bacteria. Environ Microbiol. 2010;12:28–39.
pubmed: 19691500
doi: 10.1111/j.1462-2920.2009.02027.x
Alagely A, Krediet CJ, Ritchie KB, Teplitski M. Signaling-mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens. ISME J. 2011;5:1609–20.
pubmed: 21509042
pmcid: 3176518
doi: 10.1038/ismej.2011.45
Stocker R, Seymour JR, Samadani A, Hunt DE, Polz MF. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc Natl Acad Sci U.S.A. 2008;105:4209–14.
pubmed: 18337491
pmcid: 2393791
doi: 10.1073/pnas.0709765105
Polz MF, Hunt DE, Preheim SP, Weinreich DM. Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes. Philos Trans R Soc B Biol Sci. 2006;361:2009–21.
doi: 10.1098/rstb.2006.1928
Taylor JR, Stocker R. Trade-offs of chemotactic foraging in turbulent water. Science. 2012;338:675–9.
pubmed: 23118190
doi: 10.1126/science.1219417
Krediet CJ, Ritchie KB, Cohen M, Lipp EK, Patterson Sutherland K, Teplitski M. Utilization of mucus from the coral Acropora palmata by the pathogen Serratia marcescens and by environmental and coral commensal bacteria. Appl Environ Microbiol. 2009;75:3851–8.
pubmed: 19395569
pmcid: 2698349
doi: 10.1128/AEM.00457-09
Krediet CJ, Ritchie KB, Alagely A, Teplitski M. Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen. ISME J. 2013;7:980–90.
pubmed: 23254513
doi: 10.1038/ismej.2012.164
Packer HL, Armitage JP. The chemokinetic and chemotactic behavior of Rhodobacter sphaeroides: two independent responses. J Bacteriol. 1994;176:206–12.
pubmed: 8282697
pmcid: 205032
doi: 10.1128/jb.176.1.206-212.1994
Deepika D, Karmakar R, Tirumkudulu MS, Venkatesh KV. Variation in swimming speed of Escherichia coli in response to attractant. Arch Microbiol. 2015;197:211–22.
pubmed: 25308216
doi: 10.1007/s00203-014-1044-5
Zhulin IB, Armitage JP. Motility, chemokinesis, and methylation-independent chemotaxis in Azospirillum brasilense. J Bacteriol. 1993;175:952–8.
pubmed: 8432718
pmcid: 193006
doi: 10.1128/jb.175.4.952-958.1993
Ramos HC, Rumbo M, Sirard J-C. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 2004;12:509–17.
pubmed: 15488392
doi: 10.1016/j.tim.2004.09.002
Reed KC, Muller EM, van Woesik R. Coral immunology and resistance to disease. Dis Aquat Organ. 2010;90:85–92.
pubmed: 20662364
doi: 10.3354/dao02213
Ushijima B, Videau P, Poscablo D, Stengel JW, Beurmann S, Burger AH, et al. Mutation of the toxR or mshA genes from Vibrio coralliilyticus strain OCN014 reduces infection of the coral Acropora cytherea. Environ Microbiol. 2016;18:4055–67.
pubmed: 27348808
doi: 10.1111/1462-2920.13428
Ushijima B, Richards GP, Watson MA, Schubiger CB, Häse CC. Factors affecting infection of corals and larval oysters by Vibrio coralliilyticus. PLoS ONE. 2018;13:e0199475.
pubmed: 29920567
pmcid: 6007914
doi: 10.1371/journal.pone.0199475
Peterson KM, Mekalanos JJ. Characterization of the Vibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization. Infect Immun. 1988;56:2822–9.
pubmed: 2902009
pmcid: 259656
doi: 10.1128/iai.56.11.2822-2829.1988
Provenzano D, Klose KE. Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc Natl Acad Sci U.S.A. 2000;97:10220–4.
pubmed: 10944196
pmcid: 27820
doi: 10.1073/pnas.170219997
Waters CM, Bassler BL. The Vibrio harveyi quorum-sensing system uses shared regulatory components to discriminate between multiple autoinducers. Genes Dev. 2006;20:2754–67.
pubmed: 17015436
pmcid: 1578700
doi: 10.1101/gad.1466506
Mukherjee S, Bassler BL. Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol. 2019;17:371–82.
Sikora AE, Zielke RA, Lawrence DA, Andrews PC, Sandkvist M. Proteomic analysis of the Vibrio cholerae type II secretome reveals new proteins, including three related serine proteases. J Biol Chem. 2011;286:16555–66.
pubmed: 21385872
pmcid: 3089498
doi: 10.1074/jbc.M110.211078
Korotkov KV, Sandkvist M, Hol WGJ. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol. 2012;10:336–51.
pubmed: 22466878
pmcid: 3705712
doi: 10.1038/nrmicro2762
Stathopoulos C, Hendrixson DR, Thanassi DG, Hultgren SJ, St. Geme III JW, Curtiss III R. Secretion of virulence determinants by the general secretory pathway in Gram-negative pathogens: an evolving story. Microbes Infect. 2000;2:1061–72.
Hood RD, Singh P, Hsu FS, Güvener T, Carl MA, Trinidad RRS, et al. A Type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe. 2010;7:25–37.
pubmed: 20114026
pmcid: 2831478
doi: 10.1016/j.chom.2009.12.007
Zheng J, Ho B, Mekalanos JJ. Genetic analysis of anti-amoebae and anti-bacterial activities of the Type VI secretion system in Vibrio cholerae. PLoS ONE. 2011;6:e23876.
MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki S. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci U.S.A. 2010;107:19520–4.
pubmed: 20974937
pmcid: 2984155
doi: 10.1073/pnas.1012931107
Lee SH, Hava DL, Waldor MK, Camilli A. Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell. 1999;99:625–34.
Pennetzdorfer N, Lembke M, Pressler K, Matson JS, Reidl J, Schild S. Regulated proteolysis in Vibrio cholerae allowing rapid adaptation to stress conditions. Front Cell Infect Microbiol. 2019;9:1–9.
doi: 10.3389/fcimb.2019.00214
Liu R, Chen H, Zhang R, Zhou Z, Hou Z, Gao D, et al. Comparative transcriptome analysis of Vibrio splendidus JZ6 reveals the mechanism of its pathogenicity at low temperatures. Appl Environ Microbiol. 2016;82:2050–61.
pubmed: 26801576
pmcid: 4807526
doi: 10.1128/AEM.03486-15
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science. 2018;359:80–3.
Vezzulli L, Previati M, Pruzzo C, Marchese A, Bourne DG, Cerrano C, et al. Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. Environ Microbiol. 2010;12:2007–19.
Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R, Payet JP, et al. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Commun. 2016;7:1–12.
doi: 10.1038/ncomms11833