Leisingera sp. JC1, a bacterial isolate from hawaiian bobtail squid eggs, produces indigoidine and differentially inhibits vibrios

Frontiers in Microbiology

Volumn 7, Issue SEP, 2016, Pages

  Gromek, Samantha M ^a   Suria, Andrea M ^a   Fullmer, Matthew S ^a   Garcia, Jillian L ^a   Gogarten, Johann Peter ^a   Nyholm, Spencer V ^a   Balunas, Marcy J ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

DART MS; Euprymna; Indigoidine; Leisingera; Rhodobacteraceae; Roseobacter; Secondary metabolite regulation; Symbiosis

Indexed keywords

SIDEROPHORE;

AGROBACTERIUM TUMEFACIENS; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIUM; BIOCHEMICAL ANALYSIS; BIOSYNTHESIS; COLONY FORMING UNIT; CONTROLLED STUDY; GENE CLUSTER; INHIBITION ZONE; LEISINGERA; MASS SPECTROMETRY; NONHUMAN; PHYLOGENETIC TREE; PROBABILITY; QUORUM SENSING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; VIBRIO;

EID: 84992735558     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01342     Document Type: Article

References (64)

1. Alikhan, N.-F., Petty, N. K., Ben Zakour, N. L., and Beatson, S. A. (2011). BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402. doi: 10.1186/1471-2164-12-402
2. Amsler, C. D., McClintock, J. B., and Baker, B. J. (2001). Secondary metabolites as mediators of trophic interactions among Antarctic marine organisms. Am. Zool. 41, 17-26.
3. Antonic, V., Stojadinovic, A., Zhang, B., Izadjoo, M. J., and Alavi, M. (2013). Pseudomonas aeruginosa induces pigment production and enhances virulence in a white phenotypic variant of Staphylococcus aureus. Infect. Drug Resist. 6, 175-186. doi: 10.2147/IDR.S49039
4. Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., et al. (2008). The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. doi: 10.1186/1471-2164-9-75
5. Barbieri, E., Barry, K., Child, A., and Wainwright, N. (1997). Antimicrobial activity in the microbial community of the accessory nidamental gland and egg cases of Loligo pealei (Cephalopoda: Loliginidae). Biol. Bull. 193, 275-276.
6. Barbieri, E., Paster, B., Hughes, D., Zurek, L., Moser, D., Teske, A., et al. (2001). Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda:Loliginidae). Environ. Microbiol. 3, 151-167. doi: 10.1046/j.1462-2920.2001.00172.x
7. Berger, M., Neumann, A., Schulz, S., Simon, M., and Brinkhoff, T. (2011). Tropodithietic acid production in Phaeobacter gallaeciensis is regulated by N-acyl homoserine lactone-mediated quorum sensing. J. Bacteriol. 193, 6576-6585. doi: 10.1128/JB.05818-11
8. Boettcher, K. J., Ruby, E. G., and McFall-Ngai, M. J. (1996). Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J. Comp. Physiol. 179, 65-73. doi: 10.1007/BF00193435
9. Bruhn, J. B., Gram, L., and Belas, R. (2007). Production of antibacterial compounds and biofilm formation by Roseobacter species are influenced by culture conditions. Appl. Environ. Microbiol. 73, 442-450. doi: 10.1128/AEM.02238-06
10. Bruhn, J. B., Haagensen, J. A. J., Bagge-Ravn, D., and Gram, L. (2006). Culture conditions of Roseobacter strain 27-4 affect its attachment and biofilm formation as quantified by real-time PCR. Appl. Environ. Microbiol. 72, 3011-3015. doi: 10.1128/AEM.72.4.3011-3015.2006
11. Cha, C., Gao, P., Chen, Y. C., Shaw, P. D., and Farrand, S. K. (1998). Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol. Plant Microbe Interact. 11, 1119-1129. doi: 10.1094/MPMI.1998.11.11.1119
12. Chilton, M. D., Currier, T. C., Farrand, S. K., Bendich, A. J., Gordon, M. P., and Nester, E. W. (1974). Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc. Natl. Acad. Sci. U.S.A. 71, 3672-3676. doi: 10.1073/pnas.71.9.3672
13. Cianfanelli, F. R., Monlezun, L., and Coulthurst, S. J. (2016). Aim, load, and fire: the Type VI secretion system, a bacterial nanoweapon. Trends Microbiol. 24, 51-62. doi: 10.1016/j.tim.2015.10.005
14. th Edn. Wayne, PA: Clinical and Laboratory Standards Institute.
15. Collins, A. J., Fullmer, M. S., Gogarten, J. P., and Nyholm, S. V. (2015). Comparative genomics of Roseobacter clade bacteria isolated from the accessory nidamental gland of Euprymna scolopes. Front. Microbiol. 6:123. doi: 10.3389/fmicb.2015.00123
16. Collins, A. J., LaBarre, B. A., Won, B. S., Shah, M. V., Heng, S., Choudhury, M. H., et al. (2012). Diversity and partitioning of bacterial populations within the accessory nidamental gland of the squid Euprymna scolopes. Appl. Environ. Microbiol. 78, 4200-4208. doi: 10.1128/AEM.07437-11
17. Collins, A. J., and Nyholm, S. V. (2011). Draft genome of Phaeobacter gallaeciensis ANG1, a dominant member of the accessory nidamental gland of Euprymna scolopes. J. Bacteriol. 193, 3397-3398. doi: 10.1128/JB.05139-11
18. Cude, W. N., Mooney, J., Tavanaei, A. A., Hadden, M. K., Frank, A. M., Gulvik, C. A., et al. (2012). Production of the antimicrobial secondary metabolite indigoidine contributes to competitive surface colonization by the marine Roseobacter Phaeobacter sp. strain Y4I. Appl. Environ. Microbiol. 78, 4771-4780. doi: 10.1128/AEM.00297-12
19. Cude, W. N., Prevatte, C. W., Hadden, M. K., May, A. L., Smith, R. T., Swain, C. L., et al. (2015). Phaeobacter sp. strain Y4I utilizes two separate cell-to-cell communication systems to regulate production of the antimicrobial indigoidine. Appl. Environ. Microbiol. 81, 1417-1425. doi: 10.1128/AEM.02551-14
20. Darling, A. E., Mau, B., and Perna, N. T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5:e11147. doi: 10.1371/journal.pone.0011147
21. Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772. doi: 10.1038/nmeth.2109
22. Durand, E., Cambillau, C., Cascales, E., and Journet, L. (2014). VgrG, Tae, Tle, and beyond: the versatile arsenal of Type VI secretion effectors. Trends Microbiol. 22, 498-507. doi: 10.1016/j.tim.2014.06.004
23. Edenborn, H. M., and Litchfield, C. D. (1985). Glycolate metabolism by Pseudomonas sp., strain S227, isolated from a coastal marine sediment. Mar. Bio. 88, 199-205. doi: 10.1007/BF00397167
24. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. doi: 10.1093/nar/gkh340
25. Fl�rez, L. V., Biedermann, P. H., Engl, T., and Kaltenpoth, M. (2015). Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat. Prod. Rep. 32, 904-936. doi: 10.1039/c5np00010f
26. Furrow, F. B., Amsler, C. D., McClintock, J. B., and Baker, B. J. (2003). Surface sequestration of chemical feeding deterrents in the Antarctic sponge Latrunculia apicalis as an optimal defense against sea star spongivory. Mar. Bio. 143, 443-449. doi: 10.1007/s00227-003-1109-5
27. Geng, H., Bruhn, J. B., Nielsen, K. F., Gram, L., and Belas, R. (2008). Genetic dissection of tropodithietic acid biosynthesis by marine roseobacters. Appl. Environ. Microbiol. 74, 1535-1545. doi: 10.1128/AEM.02339-07
28. Grigioni, S., Boucher-Rodoni, R., Demarta, A., Tonolla, M., and Peduzzi, R. (2000). Phylogenetic characterisation of bacterial symbionts in the accessory nidamental glands of the sepioid Sepia officinalis (Cephalopoda: Decapoda). Mar. Biol. 136, 217-222. doi: 10.1007/s002270050679
29. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321. doi: 10.1093/sysbio/syq010
30. Hood, R. D., Singh, P., Hsu, F., G�vener, T., Carl, M. A., Trinidad, R. R. S., et al. (2010). A Type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25-37. doi: 10.1016/j.chom.2009.12.007
31. Jiang, F., Waterfield, N. R., Yang, J., Yang, G., and Jin, Q. (2014). A Pseudomonas aeruginosa type VI secretion phospholipase D effector targets both prokaryotic and eukaryotic cells. Cell Host Microbe 15, 600-610. doi: 10.1016/j.chom.2014.04.010
32. Kaufman, M., Ikeda, Y., Patton, C., van Dykhuizen, G., and Epel, D. (1998). Bacterial symbionts colonize the accessory nidamental gland of the squid Loligo opalescens via horizontal transmission. Biol. Bull. 194, 36-43. doi: 10.2307/1542511
33. Martens, T., Gram, L., Grossart, H. P., Kessler, D., M�ller, R., Simon, M., et al. (2007). Bacteria of the Roseobacter clase show potential for secondary metabolite production. Microb. Ecol. 54, 31-42. doi: 10.1007/s00248-006-9165-2
34. McFall-Ngai, M. J. (2014). The importance of microbes in animal development: lessons from the squid-vibrio symbiosis. Ann. Rev. Microbiol. 68, 177-194. doi: 10.1146/annurev-micro-091313-103654
35. Meier-Kolthoff, J. P., Auch, A. F., Klenk, H.-P., and G�ker, M. (2013). Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. doi: 10.1186/1471-2105-14-60
36. Newton, R. J., Griffin, L. E., Bowles, K. M., Meile, C., Gifford, S., Givens, C. E., et al. (2010). Genome characteristics of a generalist marine bacterial lineage. ISME J. 4, 784-798. doi: 10.1038/ismej.2009.150
37. Nyholm, S. V., and McFall-Ngai, M. J. (1998). Sampling the light-organ microenvironment of Eupyrmna scolopes: description of a population of host cells in association with the bacterial symbiont Vibrio fischeri. Biol. Bull. 195, 89-97. doi: 10.2307/1542815
38. Onaka, H., Mori, Y., Igarashi, Y., and Furumai, T. (2011). Mycolic acid-containing bacteria induce natural-product biosynthesis in Streptomyces species. Appl. Environ. Microbiol. 77, 400-406. doi: 10.1128/AEM.01337-10
39. Orf, G. S., and Blankenship, R. E. (2013). Chlorosome antenna complexes from green photosynthetic bacteria. Photosynth. Res. 116, 315-331. doi: 10.1007/s11120-013-9869-3
40. Pichon, D., Gaia, V., Norman, M. D., and Boucher-Rodoni, R. (2005). Phylogenetic diversity of epibiotic bacteria in the accessory nidamental glands of squids (Cephalopoda: Loliginidae and Idiosepiidae). Mar. Biol. 147, 1323-1332. doi: 10.1007/s00227-005-0014-5
41. Pukatzki, S., Ma, A. T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W. C., et al. (2006). Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. U.S.A. 103, 1528-1533. doi: 10.1073/pnas.0510322103
42. Rao, D., Webb, J. S., Holmstr�m, C., Case, R., Low, A., Steinberg, P., et al. (2007). Low densities of epiphytic bacteria from the marine alga Ulva australis inhibit settlement of fouling organisms. Appl. Environ. Microbiol. 73, 7844-7852. doi: 10.1128/AEM.01543-07
43. Ravn, L., Christensen, A. B., Molin, S., Givskov, M., and Gram, L. (2001). Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J. Microbiol. Methods 44, 239-251. doi: 10.1016/S0167-7012(01)00217-2
44. Rice, P., Longden, I., and Bleasby, A. (2000). EMBOSS: the European molecular biology open software suite. Trends Genet. 16, 276-277. doi: 10.1016/S0168-9525(00)02024-2
45. Richter, M., and Rossell�-M�ra, R. (2009). Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. U.S.A. 106, 19126-19131. doi: 10.1073/pnas.0906412106
46. Ronquist, F., Teslenko, M., Mark, P., van der Ayres, D. L., Darling, A., H�hna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542. doi: 10.1093/sysbio/sys029
47. Ruiz, B., Ch�vez, A., Forero, A., Garc�a-Huante, Y., Romero, A., S�nchez, M., et al. (2010). Production of microbial secondary metabolites: regulation by the carbon source. Crit. Rev. Microbiol. 36, 146-167. doi: 10.3109/10408410903489576
48. Sana, T. G., Hachani, A., Bucior, I., Soscia, C., Garvis, S., Termine, E., et al. (2012). The second type VI secretion system of Pseudomonas aeruginosa strain PAO1 is regulated by quorum sensing and fur and modulates internalization in epithelial cells. J. Biol. Chem. 287, 27095-27105. doi: 10.1074/jbc. M112.376368
49. Sanchez, L. M., Curtis, M. E., Bracamonte, B. E., Kurita, K. L., Navarro, G., Sparkman, O. D., et al. (2011). Versatile method for the detection of covalently bound substrates on solid supports by DART mass spectrometry. Org. Lett. 13, 3770-3773. doi: 10.1021/ol201404v
50. Schleicher, T., and Nyholm, S. (2011). Characterizing the host and symbiont proteomes in the association between the Bobtail squid, Euprymna scolopes, and the bacterium, Vibrio fischeri. PLoS ONE 6:e25649. doi: 10.1371/journal.pone.0025649
51. Schmidt, E. W., and Donia, M. S. (2010). Life in cellulose houses: symbiotic bacterial biosynthesis of ascidian drugs and drug leads. Curr. Opin. Biotechnol. 21, 827-833. doi: 10.1016/j.copbio.2010.10.006
52. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675. doi: 10.1038/nmeth.2089
53. Schwarz, S., Hood, R. D., and Mougous, J. D. (2010). What is type VI secretion doing in all those bugs? Trends Microbiol. 18, 531-537. doi: 10.1016/j.tim.2010.09.001
54. Seyedsayamdost, M. R., Case, R. J., Kolter, R., and Clardy, J. (2011). The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat. Chem. 3, 331-335. doi: 10.1038/nchem.1002
55. Tong, Y. Y., and Lighthart, B. (1997). Solar radiation is shown to select for pigmented bacteria in the ambient outdoor atmosphere. Photochem. Photobiol. 65, 103-106. doi: 10.1111/j.1751-1097.1997.tb01884.x
56. Tritt, A., Eisen, J. A., Facciotti, M. T., and Darling, A. E. (2012). An integrated pipeline for de novo assembly of microbial genomes. PLoS ONE 7:e42304. doi: 10.1371/journal.pone.0042304
57. Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., et al. (2012). Primer3-new capabilities and interfaces. Nucleic Acids Res. 40, 1-12. doi: 10.1093/nar/gks596
58. Unterweger, D., Miyata, S. T., Bachmann, V., Brooks, T. M., Mullins, T., Kostiuk, B., et al. (2014). The Vibrio cholerae type VI secretion system employs diverse effector modules for intraspecific competition. Nat. Comm. 5, 3549. doi: 10.1038/ncomms4549
59. Van Dyck, S., Flammang, P., Meriaux, C., Bonnel, D., Salzet, M., Fournier, I., et al. (2010). Localization of secondary metabolites in marine invertebrates: contribution of MALDI MSI for the study of saponins in Cuvierian tubules of H. forskali. PLoS ONE 5:e13923. doi: 10.1371/journal.pone.0013923
60. Weber, T., Blin, K., Duddela, S., Krug, D., Kim, H. U., Bruccoleri, R., et al. (2015). antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 43, W237-W243. doi: 10.1093/nar/gkv437
61. Whistler, C. A., and Ruby, E. G. (2003). GacA regulates symbiotic colonization traits of Vibrio fischeri and facilitates a beneficial association with an animal host. J. Bacteriol. 185, 7202-7212. doi: 10.1128/JB.185.24.7202
62. Yu, D., Xu, F., Valiente, J., Wang, S., and Zhan, J. (2013). An indigoidine biosynthetic gene cluster from Streptomyces chromofuscus ATCC 49982 contains an unusual IndB homologue. J. Ind. Microbiol. Biotechnol. 40, 159-168. doi: 10.1007/s10295-012-1207-9
63. Zan, J., Cicirelli, E. M., Mohamed, N. M., Sibhatu, H., Kroll, S., Choi, O., et al. (2012). A complex LuxR-LuxI type quorum sensing network in a roseobacterial marine sponge symbiont activates flagellar motility and inhibits biofilm formation. Mol. Microbiol. 85, 916-933. doi: 10.1111/j.1365-2958.2012.08149.x
64. Zgoda, J. R., and Porter, J. R. (2001). A convenient microdilution method for screening natural products against bacteria and fungi. Pharm. Biol. 39, 221-225. doi: 10.1076/phbi.39.3.221.5934