Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Neave, Matthew J ^a,b   Michell, Craig T ^a   Apprill, Amy ^b   Voolstra, Christian R ^a  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; AQUATIC SPECIES; BACTERIAL GENOME; BIOLOGY; CLASSIFICATION; GAMMAPROTEOBACTERIA; GENE ONTOLOGY; GENETIC RECOMBINATION; GENETICS; METAGENOME; METAGENOMICS; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; PROCEDURES; SYMBIOSIS;

ADAPTATION, BIOLOGICAL; AQUATIC ORGANISMS; COMPUTATIONAL BIOLOGY; GAMMAPROTEOBACTERIA; GENE ONTOLOGY; GENOME, BACTERIAL; METAGENOME; METAGENOMICS; MOLECULAR SEQUENCE ANNOTATION; PHYLOGENY; RECOMBINATION, GENETIC; SYMBIOSIS;

EID: 85009758590     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep40579     Document Type: Article

References (90)

1. Scully, E. D. et al. Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genomics 15, 1-21 (2014).
2. Goffredi, S. K. et al. Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms. ISME J. 8, 908-924 (2014).
3. Ghanbari, M., Kneifel, W. & Domig, K. J. A new view of the fish gut microbiome: Advances from next-generation sequencing. Aquaculture 448, 464-475 (2015).
4. Price, D. R. G. et al. Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts. Proc. Natl. Acad. Sci. USA 111, 320-5 (2014).
5. Futo, M., Armitage, S. A. O. & Kurtz, J. Microbiota plays a role in oral immune priming in Tribolium castaneum. Front. Microbiol. 6, 1383 (2015).
6. Nellore, A. & Fishman, J. A. The microbiome, systemic immune function, and allotransplantation. Clin. Microbiol. Rev. 29, 191-199 (2016).
7. Cheng, X.-Y. et al. Metagenomic analysis of the pinewood nematode microbiome reveals a symbiotic relationship critical for xenobiotics degradation. Sci. Rep. 3, 1869 (2013).
8. Ceja-Navarro, J. A. et al. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 6, 7618 (2015).
9. Miljkovic, M. et al. AggLb Is the largest cell-Aggregation factor from Lactobacillus paracasei subsp. paracasei BGNJ1-64, functions in collagen adhesion, and pathogen exclusion in vitro. PLoS One 10, e0126387 (2015).
10. King, K. C. et al. Rapid evolution of microbe-mediated protection against pathogens in a worm host. ISME J doi: 10.1038/ismej.2015.259 (2016).
11. Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220-230 (2012).
12. Brooks, J. F. et al. Global discovery of colonization determinants in the squid symbiont Vibrio fischeri. Proc. Natl. Acad. Sci. 111, 17284-17289 (2014).
13. McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. 110, 3229-3236 (2013).
14. Neave, M. J., Apprill, A., Ferrier-Pagès, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315-8324 (2016).
15. Morrow, K. M. et al. Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J. 9, 894-908 (2015).
16. Apprill, A., Hughen, K. & Mincer, T. Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environ. Microbiol. 15, 2063-72 (2013).
17. Ziegler, M. et al. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar. Pollut. Bull. 105, 629-640 (2016).
18. Jessen, C. et al. In-situ Effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea coral Acropora hemprichii. PLoS One 8, e62091 (2013).
19. Bayer, T. et al. The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-Associated Endozoicomonas bacteria. Appl. Environ. Microbiol. 79, 4759-4762 (2013).
20. Doepke, H., Herrmann, K. & Schuett, C. Endobacteria in the tentacles of selected cnidarian species and in the cerata of their nudibranch predators. Helgol. Mar. Res. 66, 43-50 (2012).
21. Cleary, D. F. R., Becking, L. E., Polónia, A. R. M., Freitas, R. M. & Gomes, N. C. M. Jellyfish-Associated bacterial communities and bacterioplankton in Indonesian Marine lakes. FEMS Microbiol. Ecol. doi: 10.1093/femsec/fiw064 (2016).
22. Fiore, C. L., Labrie, M., Jarett, J. K. & Lesser, M. P. Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular evidence for metabolic interchange. Front. Microbiol. 6, 364 (2015).
23. Nishijima, M., Adachi, K., Katsuta, A., Shizuri, Y. & Yamasato, K. Endozoicomonas numazuensis sp. nov., a gammaproteobacterium isolated from marine sponges, and emended description of the genus Endozoicomonas Kurahashi and Yokota 2007. Int. J. Syst. Evol. Microbiol. 63, 709-14 (2013).
24. Bayer, T. et al. Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini. Mar. Ecol. Prog. Ser. 479, 75-84 (2013).
25. La Rivière, M., Roumagnac, M., Garrabou, J. & Bally, M. Transient shifts in bacterial communities associated with the temperate gorgonian Paramuricea clavata in the Northwestern Mediterranean Sea. PLoS One 8, e57385 (2013).
26. Ransome, E., Rowley, S. J., Thomas, S., Tait, K. & Munn, C. B. Disturbance to conserved bacterial communities in the cold water gorgonian coral Eunicella verrucosa. FEMS Microbiol. Ecol. 90, 404-416 (2014).
27. Beinart, R., Nyholm, S., Dubilier, N. & Girguis, P. Intracellular Oceanospirillales inhabit the gills of the hydrothermal vent snail Alviniconcha with chemosynthetic, -proteobacterial symbionts. Environ. Microbiol. Rep. 6, 656-664 (2014).
28. Roterman, Y. R., Benayahu, Y., Reshef, L. & Gophna, U. The gill microbiota of invasive and indigenous Spondylus oysters from the Mediterranean Sea and northern Red Sea. Environ. Microbiol. Rep. 7, 860-867 (2015).
29. Forget, N. L. & Juniper, K. S. Free-living bacterial communities associated with tubeworm (Ridgeia piscesae) aggregations in contrasting diffuse flow hydrothermal vent habitats at the Main Endeavour Field, Juan de Fuca Ridge. Microbiologyopen 2, 259-75 (2013).
30. Katharios, P. et al. Environmental marine pathogen isolation using mesocosm culture of sharpsnout seabream: Striking genomic and morphological features of novel Endozoicomonas sp. Sci. Rep. 5, 17609 (2015).
31. Mendoza, M. et al. A novel agent (Endozoicomonas elysicola) responsible for epitheliocystis in cobia Rachycentrum canadum larvae. Dis. Aquat. Organ. 106, 31-7 (2013).
32. Dishaw, L. J. et al. The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS One 9, e93386 (2014).
33. Cahill, P. L., Fidler, A. E., Hopkins, G. A. & Wood, S. A. Geographically conserved microbiomes of four temperate water tunicates. Environ. Microbiol. Rep. doi: 10.1111/1758-2229.12391 (2016).
34. Pike, R. E., Haltli, B. & Kerr, R. G. Endozoicomonas euniceicola sp. nov. and Endozoicomonas gorgoniicola sp. nov., bacteria isolated from the octocorals, Eunicea fusca and Plexaura sp. Int. J. Syst. Evol. Microbiol. 63, 4294-4302 (2013).
35. Neave, M. J., Michell, C. T., Apprill, A. & Voolstra, R. Whole-genome sequences of three symbiotic Endozoicomonas strains. Genome Announc. 2, e00802-14 (2014).
36. Morrow, K. M., Moss, A. G., Chadwick, N. E. & Liles, M. R. Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl. Environ. Microbiol. 78, 6438-49 (2012).
37. Pantos, O., Bongaerts, P., Dennis, P. G., Tyson, G. W. & Hoegh-Guldberg, O. Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J. 9, 1916-1927 (2015).
38. Bourne, D. G. et al. Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J. 7, 1452-1458 (2013).
39. Bourne, D., Iida, Y., Uthicke, S. & Smith-Keune, C. Changes in coral-Associated microbial communities during a bleaching event. ISME J. 2, 350-63 (2008).
40. Ritchie, K. B. Regulation of microbial populations by coral surface mucus and mucus-Associated bacteria. Mar. Ecol. Prog. Ser. 322, 1-14 (2006).
41. Ding, J.-Y., Shiu, J.-H., Chen, W.-M., Chiang, Y.-R. & Tang, S.-L. Genomic insight into the host-endosymbiont relationship of Endozoicomonas montiporae CL-33(T) with its coral host. Front. Microbiol. 7, 251 (2016).
42. Albertsen, M. et al. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533-8 (2013).
43. La Rivière, M., Garrabou, J. & Bally, M. Evidence for host specificity among dominant bacterial symbionts in temperate gorgonian corals. Coral Reefs 34, 1087-1098 (2015).
44. Neave, M. J. et al. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J 11, 186-200 (2017).
45. Remigi, P., Zhu, J., Young, J. P. W. & Masson-Boivin, C. Symbiosis within symbiosis: Evolving nitrogen-fixing legume symbionts. Trends Microbiol. 24, 63-75 (2016).
46. Poole, P. & Allaway, D. In Advances in Microbial Physiology 43, 117-163 (Academic Press, 2000).
47. Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J. & Wild, C. Nitrogen cycling in corals: The key to understanding holobiont functioning Trends Microbiol. 23, 490-497 (2015).
48. Hansen, A. K. & Moran, N. A. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc. Natl. Acad. Sci. 108, 2849-54 (2011).
49. Deutscher, J., Francke, C. & Postma, P. W. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70, 939-1031 (2006).
50. Ymele-Leki, P., Houot, L. & Watnick, P. I. Mannitol and the mannitol-specific enzyme IIB subunit activate vibrio cholerae biofilm formation. Appl. Environ. Microbiol. 79, 4675-4683 (2013).
51. Brady, S. K., Sreelatha, S., Feng, Y., Chundawat, S. P. S. & Lang, M. J. Cellobiohydrolase 1 from Trichoderma reesei degrades cellulose in single cellobiose steps. Nat Commun 6, 10149 (2015).
52. Lux, R., Jahreis, K., Bettenbrock, K., Parkinson, J. S. & Lengeler, J. W. Coupling the phosphotransferase system and the methylaccepting chemotaxis protein-dependent chemotaxis signaling pathways of Escherichia coli. Proc. Natl. Acad. Sci. 92, 11583-11587 (1995).
53. Pereira, C. S. et al. Phosphoenolpyruvate phosphotransferase system regulates detection and processing of the quorum sensing signal autoinducer-2. Mol. Microbiol. 84, 93-104 (2012).
54. Siguier, P., Gourbeyre, E. & Chandler, M. Bacterial insertion sequences: Their genomic impact and diversity. FEMS Microbiol. Rev. 38, 865-891 (2014).
55. Cerveau, N., Leclercq, S., Leroy, E., Bouchon, D. & Cordaux, R. Short-And long-Term evolutionary dynamics of bacterial insertion sequences: Insights from Wolbachia endosymbionts. Genome Biol. Evol. 3, 1175-1186 (2011).
56. Schmitz-Esser, S. et al. The genome of the amoeba symbiont 'Candidatus Amoebophilus asiaticus' reveals common mechanisms for host cell interaction among amoeba-Associated bacteria. J. Bacteriol. 192, 1045-57 (2010).
57. Parkhill, J. et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35, 32-40 (2003).
58. Agostini, S., Suzuki, Y. & Casareto, B. Coral symbiotic complex: Hypothesis through Vitamin B12 for a new evaluation. Coral Reef 11, 1-11 (2009).
59. Agostini, S. et al. Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 31, 147-156 (2012).
60. Eren, A. M. et al. Anvi'o: An advanced analysis and visualization platform for 'omics data. PeerJ 3, e1319 (2015).
61. Imelfort, M. et al. GroopM: An automated tool for the recovery of population genomes from related metagenomes. PeerJ 2, e603 (2014).
62. Alneberg, J. et al. Binning metagenomic contigs by coverage and composition. Nat Meth 11, 1144-1146 (2014).
63. Wang, Y. & Navin, N. E. Advances and applications of single-cell sequencing technologies. Mol. Cell 58, 598-609 (2015).
64. Pernice, M. & Levy, O. Novel tools integrating metabolic and gene function to study the impact of the environment on coral symbiosis. Front. Microbiol. 5, 448 (2014).
65. Kurahashi, M. & Yokota, A. Endozoicomonas elysicola gen. nov., sp. nov., a gamma-proteobacterium isolated from the sea slug Elysia ornata. Syst. Appl. Microbiol. 30, 202-6 (2007).
66. Yang, C.-S. et al. Endozoicomonas montiporae sp. nov., isolated from the encrusting pore coral Montipora aequituberculata. Int. J. Syst. Evol. Microbiol. 60, 1158-62 (2010).
67. Wegley, L., Edwards, R., Rodriguez-Brito, B., Liu, H. & Rohwer, F. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9, 2707-19 (2007).
68. Sunagawa, S. et al. Bacterial diversity and White Plague Disease-Associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3, 512-21 (2009).
69. Rowan, R. & Powers, D. Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar. Ecol. Prog. Ser. 71, 65-73 (1991).
70. Le Goff-Vitry, M. C., Rogers, A. D. & Baglow, D. A deep-sea slant on the molecular phylogeny of the Scleractinia. Mol. Phylogenet. Evol. 30, 167-177 (2004).
71. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120 (2014).
72. Peng, Y., Leung, H. C. M., Yiu, S. M. & Chin, F. Y. L. IDBA-UD: A de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420-1428 (2012).
73. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat Meth 9, 357-359 (2012).
74. Hyatt, D. et al. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 1-11 (2010).
75. Johnson, L. S., Eddy, S. R. & Portugaly, E. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11, 431 (2010).
76. Huson, D. H., Mitra, S., Ruscheweyh, H.-J., Weber, N. & Schuster, S. C. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552-1560 (2011).
77. Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043-1055 (2015).
78. Overbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, D206-D214 (2014).
79. Stepanauskas, R. & Sieracki, M. E. Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proc. Natl. Acad. Sci. 104, 9052-9057 (2007).
80. Bankevich, A. et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-77 (2012).
81. Markowitz, V. M. et al. IMG: The integrated microbial genomes database and comparative analysis system. Nucleic Acids Res. 40, D115-D122 (2012).
82. Li, L., Stoeckert, C. J. & Roos, D. S. OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes. Genome Res. 13, 2178-2189 (2003).
83. Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
84. Castresana, J. Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis. Mol. Biol. Evol. 17, 540-552 (2000).
85. Stamatakis, A. RAxML Version 8: A tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatics 30, 1312-1313 (2014).
86. Krzywinski, M. I. et al. Circos: An information aesthetic for comparative genomics. Genome Res. 19, 1639-45 (2009).
87. Ashburner, M. et al. Gene Ontology: Tool for the unification of biology. Nat Genet 25, 25-29 (2000).
88. Benson, D. A. et al. GenBank. Nucleic Acids Res. 41, D36-D42 (2013).
89. Jones, P. et al. InterProScan 5: Genome-scale protein function classification. Bioinformatics 30, 1236-1240 (2014).
90. Alexa, A. & Rahnenfuhrer, J. topGO: Enrichment analysis for Gene Ontology. Bioconductor (2010).