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Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts
Open accessAbstract
Endozoicomonas bacteria are globally distributed and often abundantly associated with diverse marine hosts including reef-building corals, yet their function remains unknown. In this study we generated novel Endozoicomonas genomes from single cells and metagenomes obtained directly from the corals Stylophora pistillata, Pocillopora verrucosa, and Acropora humilis. We then compared these culture-independent genomes to existing genomes of bacterial isolates acquired from a sponge, sea slug, and coral to examine the functional landscape of this enigmatic genus. Sequencing and analysis of single cells and metagenomes resulted in four novel genomes with 60–76% and 81–90% genome completeness, respectively. These data also confirmed that Endozoicomonas genomes are large and are not streamlined for an obligate endosymbiotic lifestyle, implying that they have free-living stages. All genomes show an enrichment of genes associated with carbon sugar transport and utilization and protein secretion, potentially indicating that Endozoicomonas contribute to the cycling of carbohydrates and the provision of proteins to their respective hosts. Importantly, besides these commonalities, the genomes showed evidence for differential functional specificity and diversification, including genes for the production of amino acids. Given this metabolic diversity of Endozoicomonas we propose that different genotypes play disparate roles and have diversified in concert with their hosts.
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Cites
Trimmomatic: a flexible trimmer for Illumina sequence data
Bolger, A. M., Lohse, M., & Usadel, B. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu170 · Cited by 65,548
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662
Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
Stamatakis, A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu033 · Cited by 32,291
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., et al. (2012) · Journal of Computational Biology · doi:10.1089/cmb.2012.0021 · Cited by 25,987
Prodigal: prokaryotic gene recognition and translation initiation site identification
Hyatt, D., Chen, G.-L., LoCascio, P. F., Land, M. L., Larimer, F. W., & Hauser, L. J. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-119 · Cited by 12,587
Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P., & Tyson, G. W. (2015) · Genome Research · doi:10.1101/gr.186072.114 · Cited by 12,496
Circos: An information aesthetic for comparative genomics
Krzywinski, M., Schein, J., Birol, İ., Connors, J., Gascoyne, R., Horsman, D., Jones, S. J., & Marra, M. A. (2009) · Genome Research · doi:10.1101/gr.092759.109 · Cited by 10,964
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis
Castresana, J. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026334 · Cited by 10,508
InterProScan 5: genome-scale protein function classification
Jones, P., Binns, D., Chang, H.-Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., Nuka, G., et al. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu031 · Cited by 9,301
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
Li, L., Stoeckert, C. J., & Roos, D. S. (2003) · Genome Research · doi:10.1101/gr.1224503 · Cited by 5,707
Diversity, stability and resilience of the human gut microbiota
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., & Knight, R. (2012) · Nature · doi:10.1038/nature11550 · Cited by 5,533
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
Overbeek, R., Olson, R., Pusch, G. D., Olsen, G. J., Davis, J. J., Disz, T., Edwards, R. A., Gerdes, S., Parrello, B., Shukla, M., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gkt1226 · Cited by 4,524
Benson, D. A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., & Sayers, E. W. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1195 · Cited by 3,261
Peng, Y., Leung, H. C. M., Yiu, S. M., & Chin, F. Y. L. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts174 · Cited by 2,989
Binning metagenomic contigs by coverage and composition
Alneberg, J., Bjarnason, B. S., de Bruijn, I., Schirmer, M., Quick, J., Ijaz, U. Z., Lahti, L., Loman, N. J., Andersson, A. F., & Quince, C. (2014) · Nature Methods · doi:10.1038/nmeth.3103 · Cited by 2,800
Animals in a bacterial world, a new imperative for the life sciences
McFall-Ngai, M., Hadfield, M. G., Bosch, T. C. G., Carey, H. V., Domazet-Lošo, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218525110 · Cited by 2,782
Anvi’o: an advanced analysis and visualization platform for ‘omics data
Eren, A. M., Esen, Ö. C., Quince, C., Vineis, J. H., Morrison, H. G., Sogin, M. L., & Delmont, T. O. (2015) · PeerJ · doi:10.7717/peerj.1319 · Cited by 1,887
Integrative analysis of environmental sequences using MEGAN4
Huson, D. H., Mitra, S., Ruscheweyh, H.-J., Weber, N., & Schuster, S. C. (2011) · Genome Research · doi:10.1101/gr.120618.111 · Cited by 1,541
Deutscher, J., Francke, C., & Postma, P. W. (2006) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00024-06 · Cited by 1,424
Hidden Markov model speed heuristic and iterative HMM search procedure
Johnson, L. S., Eddy, S. R., & Portugaly, E. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-431 · Cited by 1,378
IMG: the integrated microbial genomes database and comparative analysis system
Markowitz, V. M., Chen, I.-M. A., Palaniappan, K., Chu, K., Szeto, E., Grechkin, Y., Ratner, A., Jacob, B., Huang, J., Williams, P., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr1044 · Cited by 1,311
Albertsen, M., Hugenholtz, P., Skarshewski, A., Nielsen, K. L., Tyson, G. W., & Nielsen, P. H. (2013) · Nature Biotechnology · doi:10.1038/nbt.2579 · Cited by 1,251
Parkhill, J., Sebaihia, M., Preston, A., Murphy, L. D., Thomson, N., Harris, D. E., Holden, M. T. G., Churcher, C. M., Bentley, S. D., Mungall, K. L., et al. (2003) · Nature Genetics · doi:10.1038/ng1227 · Cited by 1,037
Regulation of microbial populations by coral surface mucus and mucus-associated bacteria
Ritchie, K. (2006) · Marine Ecology Progress Series · doi:10.3354/meps322001 · Cited by 939
Bacterial insertion sequences: their genomic impact and diversity
Siguier, P., Gourbeyre, E., & Chandler, M. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12067 · Cited by 726
A new view of the fish gut microbiome: advances from next-generation sequencing
Ghanbari, M., Kneifel, W., & Domig, K. J. (2015) · Aquaculture · doi:10.1016/j.aquaculture.2015.06.033 · Cited by 669
Advances and Applications of Single-Cell Sequencing Technologies
Wang, Y., & Navin, N. E. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.05.005 · Cited by 618
Nitrogen cycling in corals: the key to understanding holobiont functioning?
Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J., & Wild, C. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.03.008 · Cited by 582
Self-citationMetagenomic analysis of the microbial community associated with the coral Porites astreoides
Wegley, L., Edwards, R., Rodriguez‐Brito, B., Liu, H., & Rohwer, F. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01383.x · Cited by 553
Changes in coral-associated microbial communities during a bleaching event
Bourne, D., Iida, Y., Uthicke, S., & Smith-Keune, C. (2008) · The ISME Journal · doi:10.1038/ismej.2007.112 · Cited by 547
Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee
Ceja-Navarro, J. A., Vega, F. E., Karaoz, U., Hao, Z., Jenkins, S., Lim, H. C., Kosina, P., Infante, F., Northen, T. R., & Brodie, E. L. (2015) · Nature Communications · doi:10.1038/ncomms8618 · Cited by 512
Aphid genome expression reveals host–symbiont cooperation in the production of amino acids
Hansen, A. K., & Moran, N. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013465108 · Cited by 452
Sunagawa, S., DeSantis, T. Z., Piceno, Y. M., Brodie, E. L., DeSalvo, M. K., Voolstra, C. R., Weil, E., Andersen, G. L., & Medina, M. (2009) · The ISME Journal · doi:10.1038/ismej.2008.131 · Cited by 407
Self-citationMolecular genetic identification of symbiotic dinoflagellates (zooxanthellae)
Rowan, R., & Powers, D. A. (1991) · Marine Ecology Progress Series · doi:10.3354/meps071065 · Cited by 344
Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas
Neave, M. J., Apprill, A., Ferrier-Pagès, C., & Voolstra, C. R. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7777-0 · Cited by 329
Self-citationGroopM: an automated tool for the recovery of population genomes from related metagenomes
Imelfort, M., Parks, D., Woodcroft, B. J., Dennis, P., Hugenholtz, P., & Tyson, G. W. (2014) · PeerJ · doi:10.7717/peerj.603 · Cited by 317
Bayer, T., Neave, M. J., Alsheikh-Hussain, A., Aranda, M., Yum, L. K., Mincer, T., Hughen, K., Apprill, A., & Voolstra, C. R. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.00695-13 · Cited by 297
Self-citationMorrow, K. M., Bourne, D. G., Humphrey, C., Botté, E. S., Laffy, P., Zaneveld, J., Uthicke, S., Fabricius, K. E., & Webster, N. S. (2015) · The ISME Journal · doi:10.1038/ismej.2014.188 · Cited by 292
Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time
Stepanauskas, R., & Sieracki, M. E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700496104 · Cited by 285
Neave, M. J., Rachmawati, R., Xun, L., Michell, C. T., Bourne, D. G., Apprill, A., & Voolstra, C. R. (2017) · The ISME Journal · doi:10.1038/ismej.2016.95 · Cited by 267
Self-citationZiegler, M., Roik, A., Porter, A., Zubier, K., Mudarris, M. S., Ormond, R., & Voolstra, C. R. (2016) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2015.12.045 · Cited by 246
Self-citationMorrow, K. M., Moss, A. G., Chadwick, N. E., & Liles, M. R. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.01162-12 · Cited by 234
Rapid evolution of microbe-mediated protection against pathogens in a worm host
King, K. C., Brockhurst, M. A., Vasieva, O., Paterson, S., Betts, A., Ford, S. A., Frost, C. L., Horsburgh, M. J., Haldenby, S., & Hurst, G. D. D. (2016) · The ISME Journal · doi:10.1038/ismej.2015.259 · Cited by 224
Biological and chemical characteristics of the coral gastric cavity
Agostini, S., Suzuki, Y., Higuchi, T., Casareto, B. E., Yoshinaga, K., Nakano, Y., & Fujimura, H. (2012) · Coral Reefs · doi:10.1007/s00338-011-0831-6 · Cited by 166
Patterns and possible environmental controls of skeletogenesis of Porites lutea, South Thailand
Scoffin, T. P., Tudhope, A. W., Brown, B. E., Chansang, H., & Cheeney, R. F. (1992) · Coral Reefs · doi:10.1007/bf00291929 · Cited by 164
Schmitz‐Esser, S., Tischler, P., Arnold, R. R., Montanaro, J., Wagner, M., Rattei, T., & Horn, M. (2009) · Journal of Bacteriology · doi:10.1128/jb.01379-09 · Cited by 160
Lux, R., Jahreis, K., Bettenbrock, K., Parkinson, J. S., & Lengeler, J. W. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.25.11583 · Cited by 150
Pantos, O., Bongaerts, P., Dennis, P. G., Tyson, G. W., & Hoegh‐Guldberg, O. (2015) · The ISME Journal · doi:10.1038/ismej.2015.3 · Cited by 143
Bayer, T., Arif, C., Ferrier‐Pagès, C., Zoccola, D., Aranda, M., & Voolstra, C. R. (2012) · Marine Ecology Progress Series · doi:10.3354/meps10197 · Cited by 142
Self-citationScully, E. D., Geib, S. M., Carlson, J. E., Tien, M., McKenna, D. D., & Hoover, K. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-1096 · Cited by 136
Jessen, C., Lizcano, J. F. V., Bayer, T., Roder, C. M., Aranda, M., Wild, C., & Voolstra, C. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062091 · Cited by 136
Self-citationFiore, C. L., Labrie, M. S., Jarett, J. K., & Lesser, M. P. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00364 · Cited by 131
Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts
Price, D. R. G., Feng, H., Baker, J. D., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306068111 · Cited by 128
Global discovery of colonization determinants in the squid symbiont Vibrio fischeri
Brooks, J. F., Gyllborg, M. C., Cronin, D. C., Quillin, S. J., Mallama, C. A., Foxall, R. L., Whistler, C. A., Goodman, A. L., & Mandel, M. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415957111 · Cited by 122
The Gut of Geographically Disparate Ciona intestinalis Harbors a Core Microbiota
Dishaw, L. J., Flores-Torres, J., Lax, S. M., Gemayel, K. T., Leigh, B. A., Melillo, D., Mueller, M. G., Natale, L., Zucchetti, I., Santis, R. D., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093386 · Cited by 119
Ding, J., Shiu, J., Chen, W., Chiang, Y., & Tang, S. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00251 · Cited by 118
A deep-sea slant on the molecular phylogeny of the Scleractinia
Goff-Vitry, M. C. L., Rogers, A. D., & Baglow, D. (2003) · Molecular Phylogenetics and Evolution · doi:10.1016/s1055-7903(03)00162-3 · Cited by 110
Cheng, X., Tian, X., Wang, Y., Lin, R.-M., Mao, Z., Chen, N., & Xie, B. (2013) · Scientific Reports · doi:10.1038/srep01869 · Cited by 101
Cellobiohydrolase 1 from Trichoderma reesei degrades cellulose in single cellobiose steps
Brady, S. K., Sreelatha, S., Feng, Y., Chundawat, S. P. S., & Lang, M. J. (2015) · Nature Communications · doi:10.1038/ncomms10149 · Cited by 86
Pereira, C. S., Santos, A. J. M., Bejerano‐Sagie, M., Correia, P. B., Marques, J. C., & Xavier, K. B. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08010.x · Cited by 82
Pike, R. E., Haltli, B., & Kerr, R. G. (2013) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.051490-0 · Cited by 77
Rivière, M. L., Roumagnac, M., Garrabou, J., & Bally, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057385 · Cited by 74
Cerveau, N., Leclercq, S., Leroy, E., Bouchon, D., & Cordaux, R. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr096 · Cited by 74
Katharios, P., Seth-Smith, H. M. B., Fehr, A. G. J., Mateos, J. M., Qi, W., Richter, D., Nufer, L., Ruetten, M., Soto, M. G., Ziegler, U., et al. (2015) · Scientific Reports · doi:10.1038/srep17609 · Cited by 74
Overby, C. L., Tarczy-Hornoch, P. Z., Hoath, J. I., Kalet, I. J., & Veenstra, D. L. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-s9-s10 · Cited by 73
Mendoza, M., Güiza, L., Martinez, X., Caraballo, X., Rojas, J., Aranguren, L., & Salazar, M. (2013) · Diseases of Aquatic Organisms · doi:10.3354/dao02636 · Cited by 59
Evidence for host specificity among dominant bacterial symbionts in temperate gorgonian corals
Rivière, M. L., Garrabou, J., & Bally, M. (2015) · Coral Reefs · doi:10.1007/s00338-015-1334-7 · Cited by 58
Disturbance to conserved bacterial communities in the cold-water gorgonian coralEunicella verrucosa
Ransome, E. J., Rowley, S. J., Thomas, S. F., Tait, K., & Munn, C. B. (2014) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12398 · Cited by 55
Miljković, M., Strahinić, I., Tolinački, M., Živković, M., Kojić, S., Golić, N., & Kojić, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126387 · Cited by 54
The Microbiome, Systemic Immune Function, and Allotransplantation
Nellore, A., & Fishman, J. A. (2015) · Clinical Microbiology Reviews · doi:10.1128/cmr.00063-15 · Cited by 54
Forget, N. L., & Juniper, S. K. (2013) · MicrobiologyOpen · doi:10.1002/mbo3.70 · Cited by 45
Mannitol and the Mannitol-Specific Enzyme IIB Subunit Activate Vibrio cholerae Biofilm Formation
Ymele‐Leki, P., Houot, L., & Watnick, P. I. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01184-13 · Cited by 44
Coral symbiotic complex: Hypothesis through vitamin B12 for a new evaluation
Agostini, S., Suzuki, Y., Casareto, B. E., Nakano, Y., Hidaka, M., & Nesa, B. (2009) · Galaxea Journal of Coral Reef Studies · doi:10.3755/galaxea.11.1 · Cited by 42
Geographically conserved microbiomes of four temperate water tunicates
Cahill, P. L., Fidler, A. E., Hopkins, G. A., & Wood, S. A. (2016) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12391 · Cited by 42
Goffredi, S. K., Yi, H., Zhang, Q., Klann, J. E., Struve, I. A., Vrijenhoek, R. C., & Brown, C. T. (2013) · The ISME Journal · doi:10.1038/ismej.2013.201 · Cited by 40
Jellyfish-associated bacterial communities and bacterioplankton in Indonesian Marine lakes
Cleary, D. F. R., Becking, L. E., Polónia, A. R. M., Freitas, R., & Gomes, N. C. M. (2016) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiw064 · Cited by 38
Roterman, Y. R., Benayahu, Y., Reshef, L., & Gophna, U. (2015) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12315 · Cited by 34
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Self-citation
Metadata
- Authors
- Neave, M. J., Michell, C. T., Apprill, A., & Voolstra, C. R.
- Venue
- Scientific Reports
- Published
- 2017-01-17
- Volume
- 7
- Issue
- 1
- Pages
- 40579-40579
- ISSN
- 2045-2322 (ISSN-L)
- OpenAlex
- W2573866986
- Cited by
- 264
- References
- 79
- FWCI
- 16.03
- Type
- journal article
- Language
- en
- Open access
- gold
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