Assessment of a metaviromic dataset generated from nearshore Lake Michigan
Siobhan C. Watkins A D , Neil Kuehnle A , C. Anthony Ruggeri A , Kema Malki A , Katherine Bruder A , Jinan Elayyan A , Kristina Damisch A , Naushin Vahora A , Paul O’Malley A , Brieanne Ruggles-Sage A , Zachary Romer B and Catherine Putonti A B C
+ Author Affiliations
- Author Affiliations
A Department of Biology, Loyola University Chicago, 1032 W. Sheridan Road, Chicago, IL 60660, USA.
B Department of Computer Science, Loyola University Chicago, Chicago, IL 60611, USA.
C Bioinformatics Program, Loyola University Chicago, Chicago, IL 60660, USA.
D Corresponding author. Email: swatkins@luc.edu
Marine and Freshwater Research 67(11) 1700-1708 https://doi.org/10.1071/MF15172
Submitted: 30 April 2015 Accepted: 6 August 2015 Published: 4 November 2015
Abstract
Bacteriophages are powerful ecosystem engineers. They drive bacterial mortality rates and genetic diversity, and affect microbially mediated biogeochemical processes on a global scale. This has been demonstrated in marine environments; however, phage communities have been less studied in freshwaters, despite representing a potentially more diverse environment. Lake Michigan is one of the largest bodies of freshwater on the planet, yet to date the diversity of its phages has yet to be examined. Here, we present a composite survey of viral ecology in the nearshore waters of Lake Michigan. Sequence analysis was performed using a web server previously used to analyse similar data. Our results revealed a diverse community of DNA phages, largely comprising the order Caudovirales. Within the scope of the current study, the Lake Michigan virome demonstrates a distinct community. Although several phages appeared to hold dominance, further examination highlighted the importance of interrogating metagenomic data at the genome level. We present our study as baseline information for further examination of the ecology of the lake. In the current study we discuss our results and highlight issues of data analysis which may be important for freshwater studies particularly, in light of the complexities associated with examining phage ecology generally.
References
Angly, F., Felts, B., Breitbart, M., Salamon, P., Edwards, R., Carlson, C., Chan, A., Haynes, M., Kelley, S., Liu, H., Mahaffy, J., Mueller, J., Nulton, J., Olson, R., Parsons, R., Rayhawk, S., Suttle, C., and Rohwer, F. (2006). The marine viromes of four oceanic regions. PLoS Biology 4, e368.| The marine viromes of four oceanic regions.Crossref | GoogleScholarGoogle Scholar | 17090214PubMed |
Angly, F., Willner, D., Prieto-Davó, A., Edwards, R., Schmieder, R., Vega-Thurber, R., Antonopoulos, D., Barott, K., Cottrell, M., Desnues, C., Dinsdale, E., Furlan, M., Haynes, M., Henn, M., Hu, Y., Kirchman, D., McDole, T., McPherson, J., Meyer, F., Miller, R., Mundt, E., Naviaux, R., Rodriguez-Mueller, B., Stevens, R., Wegley, L., Zhang, L., Zhu, B., and Rohwer, F. (2009). The GAAS metagenomic tool and its estimations of viral and microbial average genome size in four major biomes. PLoS Computational Biology 5, e1000593.
| The GAAS metagenomic tool and its estimations of viral and microbial average genome size in four major biomes.Crossref | GoogleScholarGoogle Scholar | 20011103PubMed |
Baker, A., Goddard, V., Davy, J., Schroeder, D., Adams, D., and Wilson, W. (2006). Identification of a diagnostic marker to detect freshwater cyanophages of filamentous cyanobacteria. Applied and Environmental Microbiology 72, 5713–5719.
| Identification of a diagnostic marker to detect freshwater cyanophages of filamentous cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVKjsrs%3D&md5=43b9153389f52644ebbb7511a299423bCAS | 16957185PubMed |
Berdjeb, L., Pollet, T., Chardon, C., and Jacquet, S. (2013). Spatio-temporal changes in the structure of archaeal communities in two deep freshwater lakes. FEMS Microbiology Ecology 86, 215–230.
| Spatio-temporal changes in the structure of archaeal communities in two deep freshwater lakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1eksb7K&md5=c260c79ee27411b1910d1bb9f21dedf4CAS | 23730709PubMed |
Berman-Frank, I., Lundgren, P., and Falkowski, P. (2003). Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Research in Microbiology 154, 157–164.
| Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFCjs78%3D&md5=c0f5f94a24cfced498aa2cd0f12b23b1CAS | 12706503PubMed |
Besemer, J., Lomsadze, A., and Borodovsky, M. (2001). GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Research 29, 2607–2618.
| GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltlOqtr0%3D&md5=da8929f57bd1cf4db6cd642d7ed87ed5CAS | 11410670PubMed |
Buckling, A., and Rainey, P. B. (2002). Antagonistic coevolution between a bacterium and a bacteriophage. Proceedings of the Royal Society of London B: Biological Sciences 269, 931–936.
| Antagonistic coevolution between a bacterium and a bacteriophage.Crossref | GoogleScholarGoogle Scholar |
Casjens, S. (2003). Prophages and bacterial genomics: what have we learned so far? Molecular Microbiology 49, 277–300.
| Prophages and bacterial genomics: what have we learned so far?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlslGiu70%3D&md5=a0c348a8fcdb7311bac31b32d7133763CAS | 12886937PubMed |
Clokie, M., Shan, J., Bailey, S., Jia, Y., Krisch, H., West, S., and Mann, N. (2006). Transcription of a ‘photosynthetic’ T4-type phage during infection of a marine cyanobacterium. Environmental Microbiology 8, 827–835.
| Transcription of a ‘photosynthetic’ T4-type phage during infection of a marine cyanobacterium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVekurw%3D&md5=bc665eb1d5eb551271af34aabd2b30a9CAS | 16623740PubMed |
Djikeng, A., Kuzmickas, R., Anderson, N., and Spiro, D. (2009). Metagenomic analysis of RNA viruses in a fresh water lake. PLoS One 4, e7264.
| Metagenomic analysis of RNA viruses in a fresh water lake.Crossref | GoogleScholarGoogle Scholar | 19787045PubMed |
Evans, M. A., Fahnenstiel, G., and Scavia, D. (2011). Incidental oligotrophication of North American Great Lakes. Environmental Science & Technology 45, 3297–3303.
| Incidental oligotrophication of North American Great Lakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsVygtrs%3D&md5=e9f85507e4b1837c52ebc55f8bd6976bCAS |
Fierer, N., Breitbart, M., Nulton, J., Salamon, P., Lozupone, C., Jones, R., Robeson, M., Edwards, R. A., Felts, B., Rayhawk, S., Knight, R., Rohwer, F., and Jackson, R. B. (2007). Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Applied and Environmental Microbiology 73, 7059–7066.
| Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSksLfJ&md5=7465089cb76fd0640355287f149c5e36CAS | 17827313PubMed |
Folkmanis, A., Maltzmann, W., Mellon, P., Skalka, A., and Echols, H. (1977). The essential role of the cro gene in lytic development by bacteriophage ʎ. Virology 81, 352–362.
| The essential role of the cro gene in lytic development by bacteriophage ʎ.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXlsVymtro%3D&md5=abb4d2c60442fe4040d46bae18749366CAS | 898664PubMed |
Friedrich, N., Torrents, E., Gibb, E. A., Sahlin, M., Sjöberg, B.-M., and Edgell, D. R. (2007). Insertion of a homing endonuclease creates a genes-in-pieces ribonucleotide reductase that retains function. Proceedings of the National Academy of Sciences of the United States of America 104, 6176–6181.
| Insertion of a homing endonuclease creates a genes-in-pieces ribonucleotide reductase that retains function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXks1artbs%3D&md5=24a1d0325aee8631fb166e4629d39825CAS | 17395719PubMed |
Gao, E.-B., Gui, J.-F., and Zhang, Q.-Y. (2012). A novel cyanophage with a cyanobacterial nonbleaching protein A gene in the genome. Journal of Virology 86, 236–245.
| A novel cyanophage with a cyanobacterial nonbleaching protein A gene in the genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmsVKksr4%3D&md5=50daec2f34ac40409bc9c5e4c6a61646CAS | 22031930PubMed |
Ghai, R., Mizuno, C., Picazo, A., Camacho, A., and Rodriguez‐Valera, F. (2014). Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing. Molecular Ecology 23, 6073–6090.
| Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFOgt7bK&md5=9549b1358e883643c739893af348f51bCAS | 25355242PubMed |
Gijs Kuenen, J. (2008). Anammox bacteria: from discovery to application. Nature 6, 320–326.
Hurwitz, B., and Sullivan, M. (2013). The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS One 8, e57355.
| The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFKhsr8%3D&md5=e2b4a93ef64609b45ca38219125d986dCAS | 23468974PubMed |
Ivanikova, N., Popels, L., McKay, R., and Bullerjahn, G. (2007). Lake Superior supports novel clusters of cyanobacterial picoplankton. Applied and Environmental Microbiology 73, 4055–4065.
| Lake Superior supports novel clusters of cyanobacterial picoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVOgtL0%3D&md5=03e6c0c30326ea8b4d52e74187b7faafCAS | 17468271PubMed |
Kim, K.-H., and Bae, J.-W. (2011). Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Applied and Environmental Microbiology 77, 7663–7668.
| Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Ors7jM&md5=464a1a5cc612c16c7697cca16a7ea3e4CAS | 21926223PubMed |
Kimura, S., Sako, Y., and Yoshida, T. (2013). Rapid Microcystis cyanophage gene diversification revealed by long- and short-term genetic analyses of the tail sheath gene in a natural pond. Applied and Environmental Microbiology 79, 2789–2795.
| Rapid Microcystis cyanophage gene diversification revealed by long- and short-term genetic analyses of the tail sheath gene in a natural pond.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVKltL0%3D&md5=86f1b8265c4f199fefb3f1f0f0cdf1b7CAS | 23417006PubMed |
Kristensen, D., Waller, A., Yamada, T., Bork, P., Mushegian, A., and Koonin, E. (2013). Orthologous gene clusters and taxon signature genes for viruses of prokaryotes. Journal of Bacteriology 195, 941–950.
| Orthologous gene clusters and taxon signature genes for viruses of prokaryotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltV2iurk%3D&md5=a8604c186f14771a614eeddcdf8111c0CAS | 23222723PubMed |
Maranger, R., and Bird, D. (1995). Viral abundance in aquatic systems: a comparison between marine and fresh waters. Marine Ecology Progress Series 121, 217–226.
| Viral abundance in aquatic systems: a comparison between marine and fresh waters.Crossref | GoogleScholarGoogle Scholar |
Marchesi, J., Weightman, A., Cragg, B., Parkes, R., and Fry, J. (2001). Methanogen and bacterial diversity and distribution in deep gas hydrate sediments from the Cascadia Margin as revealed by 16S rRNA molecular analysis. FEMS Microbiology Ecology 34, 221–228.
| Methanogen and bacterial diversity and distribution in deep gas hydrate sediments from the Cascadia Margin as revealed by 16S rRNA molecular analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXht1Ghur8%3D&md5=999b76847d134da20efde5ac99f2e3afCAS | 11137602PubMed |
Minot, S., Sinha, R., Chen, J., Hongzhe, Li., Keilbaugh, S. A., Wu, G. D., Lewis, J. D., and Bushman, F. D. (2011). The human gut virome: inter-individual variation and dynamic response to diet. Genome Research 21, 1616–1625.
| The human gut virome: inter-individual variation and dynamic response to diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlSru77P&md5=038bfd5b280bc98d65193e89434028eeCAS | 21880779PubMed |
Namiki, T., Hachiya, T., Tanaka, H., and Sakakibara, Y. (2012). MetaVelvet: an extension of Velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Research 40, e155.
| MetaVelvet: an extension of Velvet assembler to de novo metagenome assembly from short sequence reads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Wqtr7F&md5=f673bd73cd55251f979377143749311fCAS | 22821567PubMed |
Newton, R., Jones, S., Eiler, A., McMahon, K., and Bertilsson, S. (2011). A guide to the natural history of freshwater lake bacteria. Microbiology and Molecular Biology Reviews 75, 14–49.
| A guide to the natural history of freshwater lake bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVequ74%3D&md5=a04870d526966dfe21a20534abcac48dCAS | 21372319PubMed |
Ondov, B., Bergman, N., and Phillippy, A. (2011). Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12, 385–394.
| Interactive metagenomic visualization in a Web browser.Crossref | GoogleScholarGoogle Scholar | 21961884PubMed |
Pilcher, D. J., McKinley, G. A., Bootsma, H. A., and Bennington, V. (2015). Physical and biogeochemical mechanisms of internal carbon cycling in Lake Michigan. Journal of Geophysical Research 120, 2112–2128.
| 1:CAS:528:DC%2BC2MXmsFygsL8%3D&md5=389dae5d6c33fdc359fec62c929303afCAS |
Poretsky, R., Rodriguez-R, L., Luo, C., Tsementzi, D., and Konstantinidis, K. (2014). Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS One 9, e93827.
| Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics.Crossref | GoogleScholarGoogle Scholar | 24714158PubMed |
Reyes, A., Semenkovich, N., Whiteson, K., Rohwer, F., and Gordon, J. (2012). Going viral: next-generation sequencing applied to phage populations in the human gut. Nature Reviews. Microbiology 10, 607–617.
| Going viral: next-generation sequencing applied to phage populations in the human gut.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFCrt7jM&md5=1f2d5a206e45092cbcd8fbba7f6d3b2cCAS | 22864264PubMed |
Rice, G., Tang, L., Stedman, K., Roberto, F., Spuhler, J., Gillitzer, E., Johnson, J., Douglas, T., and Young, M. (2004). The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life. Proceedings of the National Academy of Sciences of the United States of America 101, 7716–7720.
| The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOlurk%3D&md5=c078b94cda68a9c18ffbf96e8e292aaeCAS | 15123802PubMed |
Roux, S., Faubladier, M., Mahul, A., Paulhe, N., Bernard, A., Debroas, D., and Enault, F. (2011). Metavir: a web server dedicated to virome analysis. Bioinformatics 27, 3074–3075.
| Metavir: a web server dedicated to virome analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGkur%2FI&md5=318b05af50921e73086a26d2788eae6fCAS | 21911332PubMed |
Roux, S., Enault, F., Robin, A., Ravet, V., Personnic, S., Theil, S., Colombet, J., Sime-Ngando, T., and Debroas, D. (2012). Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS One 7, e33641.
| Assessing the diversity and specificity of two freshwater viral communities through metagenomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xks1KisLg%3D&md5=998665b97fa08bc1dd5c01bbc11735caCAS | 22432038PubMed |
Schoenfeld, T., Liles, M., Wommack, K., Polson, S., Godiska, R., and Mead, D. (2010). Functional viral metagenomics and the next generation of molecular tools. Trends in Microbiology 18, 20–29.
| Functional viral metagenomics and the next generation of molecular tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVKm&md5=1ece80bf645488fe376246cab3077340CAS | 19896852PubMed |
Sullivan, M., Coleman, M., Weigele, P., Rohwer, F., and Chisholm, S. (2005). Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biology 3, e144.
| Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations.Crossref | GoogleScholarGoogle Scholar | 15828858PubMed |
Summer, E., Gonzalez, C., Bomer, M., Carlile, T., Embry, A., Kucherka, A., Lee, J., Mebane, L., Morrison, W., Mark, L., King, M., LiPuma, J., Vidaver, A., and Young, R. (2006). Divergence and mosaicism among virulent soil phages of the Burkholderia cepacia complex. Journal of Bacteriology 188, 255–268.
| Divergence and mosaicism among virulent soil phages of the Burkholderia cepacia complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFWru74%3D&md5=7701f98968d17aba9d9c773a8d7366c5CAS | 16352842PubMed |
Suttle, C. (2005). Viruses in the sea. Nature 437, 356–361.
| Viruses in the sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFOrtLY%3D&md5=a7120e84decea3d6a7bd29ecc3a1a671CAS | 16163346PubMed |
Wang, Y., Sheng, H.-F., He, Y., Wu, J.-Y., Jiang, Y.-X., Tam, N., and Zhou, H.-W. (2012). Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Applied and Environmental Microbiology 78, 8264–8271.
| Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1yktrrF&md5=6eb65d192954356ba81b50438de97cb0CAS | 23001654PubMed |
Watkins, S., Smith, J., Hayes, P., and Watts, J. (2014). Characterisation of host growth after infection with a broad-range freshwater cyanopodophage. PLoS One 9, e87339.
| Characterisation of host growth after infection with a broad-range freshwater cyanopodophage.Crossref | GoogleScholarGoogle Scholar | 24489900PubMed |
Winget, D., Helton, R., Williamson, K., Bench, S., Williamson, S., and Wommack, K. (2011). Repeating patterns of virioplankton production within an estuarine ecosystem. Proceedings of the National Academy of Sciences of the United States of America 108, 11 506–11 511.
| Repeating patterns of virioplankton production within an estuarine ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpt12mu7c%3D&md5=36ebefa962af53df075c8089a827137dCAS |
Yin, Y., and Fischer, D. (2008). Identification and investigation of ORFans in the viral world. BMC Genomics 9, 24.
| Identification and investigation of ORFans in the viral world.Crossref | GoogleScholarGoogle Scholar | 18205946PubMed |
Yurista, P. M., Kelly, J. R., Miller, S. E., and Van Alstine, J. D. (2012). Water quality and plankton in the United States nearshore waters of Lake Huron. Environmental Management 50, 664–678.
| Water quality and plankton in the United States nearshore waters of Lake Huron.Crossref | GoogleScholarGoogle Scholar | 22824959PubMed |
Zhao, Y., Temperton, B., Thrash, J., Schwalbach, M., Vergin, K., Landry, Z., Ellisman, M., Deerinck, T., Sullivan, M., and Giovannoni, S. (2013). Abundant SAR11 viruses in the ocean. Nature 494, 357–360.
| Abundant SAR11 viruses in the ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivVKjtr8%3D&md5=922f06d4a75b3fd43c53c921b9ad8b24CAS | 23407494PubMed |
