Metagenomic Analysis of Virus Diversity and Relative Abundance in a Eutrophic Freshwater Harbour
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sampling Sites and Collection
2.2. DNA Extraction and Sequencing
2.3. Metagenome Data Processing
2.4. Metagenome Data Analysis
3. Results
3.1. Virus Community Composition in Hamilton Harbour
3.2. Mimiviridae Community Composition in Hamilton Harbour
3.3. Virophage Community Composition in Hamilton Harbour
3.4. Influence of Environmental Parameters on Virus Community Composition
4. Discussion
4.1. Influence of Databases
4.2. Limitations of Inferring Virus Presence and Abundance from Metagenomic Datasets
4.3. Physiochemical Factors
4.4. The Virophages
4.5. Ecological Relevance
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Jacquet, S.; Miki, T.; Noble, R.; Peduzzi, P.; Wilhelm, S. Viruses in aquatic ecosystems: Important advancements of the last 20 years and prospects for the future in the field of microbial oceanography and limnology. Adv. Oceanogr. Limnol. 2010, 1, 97–141. [Google Scholar] [CrossRef]
- Bergh, O.; Borsheim, K.Y.; Bratbak, G.; Heldal, M. High abundance of viruses found in aquatic environments. Nature 1989, 340, 467–468. [Google Scholar] [CrossRef] [PubMed]
- Wommack, K.E.; Bhavsar, J.; Polson, S.W.; Chen, J.; Dumas, M.; Srinivasiah, S.; Furman, M.; Jamindar, S.; Nasko, D.J. VIROME: A standard operating procedure for analysis of viral metagenome sequences. Stand. Genom. Sci. 2012, 6, 421–433. [Google Scholar] [CrossRef] [PubMed]
- Breitbart, M.; Salamon, P.; Andresen, B.; Mahaffy, J.M.; Segall, A.M.; Mead, D.; Azam, F.; Rohwer, F. Genomic analysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. USA 2002, 99, 14250–14255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brum, J.R.; Sullivan, M.B. Rising to the challenge: Accelerated pace of discovery transforms marine virology. Nat. Rev. Microbiol. 2015, 13, 147–159. [Google Scholar] [CrossRef] [PubMed]
- Brum, J.R.; Ignacio-Espinoza, J.C.; Roux, S.; Doulcier, G.; Acinas, S.G.; Alberti, A.; Chaffron, S.; Cruaud, C.; de Vargas, C.; Gasol, J.M.; et al. Patterns and ecological drivers of ocean viral communities. Science 2015, 348, 1261498. [Google Scholar] [CrossRef] [Green Version]
- De Vargas, C.; Audic, S.; Henry, N.; Decelle, J.; Mahe, F.; Logares, R.; Lara, E.; Berney, C.; Le Bescot, N.; Probert, I.; et al. Eukaryotic plankton diversity in the sunlit ocean. Science 2015, 348, 1261605. [Google Scholar] [CrossRef] [Green Version]
- Lima-Mendez, G.; Faust, K.; Henry, N.; Decelle, J.; Colin, S.; Carcillo, F.; Chaffron, S.; Ignacio-Espinosa, J.C.; Roux, S.; Vincent, F.; et al. Determinants of community structure in the global plankton interactome. Science 2015, 348, 1262073. [Google Scholar] [CrossRef]
- Sunagawa, S.; Coelho, L.P.; Chaffron, S.; Kultima, J.R.; Labadie, K.; Salazar, G.; Djahanschiri, B.; Zeller, G.; Mende, D.R.; Alberti, A.; et al. Structure and function of the global ocean microbiome. Science 2015, 348, 1261359. [Google Scholar] [CrossRef] [Green Version]
- Villar, E.; Farrant, G.K.; Follows, M.; Garczarek, L.; Speich, S.; Audic, S.; Bittner, L.; Blanke, B.; Brum, J.R.; Brunet, C.; et al. Environmental characteristics of Agulhas rings affect interocean plankton transport. Science 2015, 348, 1261447. [Google Scholar] [CrossRef] [Green Version]
- Breitbart, M.; Rohwer, F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 2005, 13, 278–284. [Google Scholar] [CrossRef] [PubMed]
- Hingamp, P.; Grimsley, N.; Acinas, S.G.; Clerissi, C.; Subirana, L.; Poulain, J.; Ferrera, I.; Sarmento, H.; Villar, E.; Lima-Mendez, G.; et al. Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J. 2013, 7, 1678–1695. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duarte, C.M. Seafaring in the 21st Century: The Malaspina 2010 Circumnavigation Expedition. Limnol Oceanogr. Bull. 2015, 24, 11–14. [Google Scholar] [CrossRef]
- Roux, S.; Brum, J.R.; Dutilh, B.E.; Sunagawa, S.; Duhaime, M.B.; Loy, A.; Poulos, B.T.; Solonenko, N.; Lara, E.; Poulain, J.; et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 2016, 537, 689–693. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Djikeng, A.; Kuzmickas, R.; Anderson, N.G.; Spiro, D.J. Metagenomic Analysis of RNA Viruses in a Fresh Water Lake. PLoS ONE 2009, 4, e7264. [Google Scholar] [CrossRef] [PubMed]
- Hewson, I.; Barbosa, J.G.; Brown, J.M.; Donelan, R.P.; Eaglesham, J.B.; Eggleston, E.M.; LaBarre, B.A. Temporal Dynamics and Decay of Putatively Allochthonous and Autochthonous Viral Genotypes in Contrasting Freshwater Lakes. Appl. Environ. Microbiol. 2012, 78, 6583–6591. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roux, S.; Enault, F.; Robin, A.; Ravet, V.; Personnic, S.; Theil, S.; Colombet, J.; Sime-Ngando, T.; Debroas, D. Assessing the Diversity and Specificity of Two Freshwater Viral Communities through Metagenomics. PLoS ONE 2012, 7, e33641. [Google Scholar] [CrossRef] [PubMed]
- De Carcer, D.A.; Lopez-Bueno, A.; Pearce, D.A.; Alcami, A. Biodiversity and distribution of polar freshwater DNA viruses. Sci. Adv. 2015, 1, e1400127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohiuddin, M.; Schellhorn, H.E. Spatial and temporal dynamics of virus occurrence in two freshwater lakes captured through metagenomic analysis. Front. Microbiol. 2015, 6, 960. [Google Scholar] [CrossRef] [Green Version]
- Green, J.C.; Rahman, F.; Saxton, M.A.; Williamson, K.E. Metagenomic assessment of viral diversity in Lake Matoaka, a temperate, eutrophic freshwater lake in southeastern Virginia, USA. Aquat. Microb. Ecol. 2015, 75, 117–128. [Google Scholar] [CrossRef]
- Sible, E.; Cooper, A.; Malki, K.; Bruder, K.; Watkins, S.C.; Fofanov, Y.; Putonti, C. Survey of viral populations within Lake Michigan nearshore waters at four Chicago area beaches. Data Brief 2015, 5, 9–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Skvortsov, T.; de Leeuwe, C.; Quinn, J.P.; McGrath, J.W.; Allen, C.C.; McElarney, Y.; Watson, C.; Arkhipova, K.; Lavigne, R.; Kulakov, L.A. Metagenomic Characterisation of the Viral Community of Lough Neagh, the Largest Freshwater Lake in Ireland. PLoS ONE 2016, 11, e0150361. [Google Scholar] [CrossRef] [PubMed]
- Ge, X.; Wu, Y.; Wang, M.; Wang, J.; Wu, L.; Yang, X.; Zhang, Y.; Shi, Z. Viral metagenomics analysis of planktonic viruses in East Lake, Wuhan, China. Virol. Sin. 2013, 28, 280–290. [Google Scholar] [CrossRef] [PubMed]
- De Carcer, D.A.; Lopez-Bueno, A.; Alonso-Lobo, J.M.; Quesada, A.; Alcami, A. Metagenomic analysis of lacustrine viral diversity along a latitudinal transect of the Antarctic Peninsula. FEMS Microbiol. Ecol. 2016, 92, fiw074. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lopez-Bueno, A.; Tamames, J.; Velazquez, D.; Moya, A.; Quesada, A.; Alcami, A. High Diversity of the Viral Community from an Antarctic Lake. Science 2009, 326, 858–861. [Google Scholar] [CrossRef] [PubMed]
- Roux, S.; Chan, L.K.; Egan, R.; Malmstrom, R.R.; McMahon, K.D.; Sullivan, M.B. Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics. Nat. Commun. 2017, 8, 858. [Google Scholar] [CrossRef] [PubMed]
- Lawrence, G.; Pieters, R.; Zaremba, L.; Tedford, T.; Gu, L.; Greco, S.; Hamblin, P. Summer exchange between Hamilton Harbour and Lake Ontario. Deep Sea Res. Part II Top. Stud. Oceanogr. 2004, 51, 475–487. [Google Scholar] [CrossRef]
- CPCS. Hamilton’s Working Waterfront: Port of Hamilton Economic Impact Study. 2016. Available online: https://economy.hamiltonport.ca/wp-content/uploads/2016/11/PortOfHamilton_Economic_Impact_Report_Oct_2016.pdf (accessed on 16 August 2018).
- IJC. Report on the Ongoing Remedial and Preventive Efforts by Responsible Governments and Organizations Relative to Restoring Hamilton Harbour. 1999. Available online: http://ijc.org/php/publications/html/hamhar/hamharsa.html (accessed on 16 August 2018).
- Poulton, D.J. Trace Contaminant Status of Hamilton Harbour. J. Great Lakes Res. 1987, 13, 193–201. [Google Scholar] [CrossRef]
- ECCC. Canadian Environmental Sustainability Indicators: Restoring the Great Lakes Areas of Concern. 2018. Available online: www.canada.ca/en/environment-climate-change/services/environmentalindicators/restoring-great-lakes-areas-concern.html (accessed on 18 August 2018).
- Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data. 2010. Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (accessed on 24 February 2018).
- Joshi, N.A.; Fass, J.N. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33) [Software]. 2011. Available online: https://github.com/najoshi/sickle (accessed on 24 February 2018).
- 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 2012, 28, 1420–1428. [Google Scholar] [CrossRef]
- Buchfink, B.; Xie, C.; Huson, D.H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 2015, 12, 59–63. [Google Scholar] [CrossRef]
- Huson, D.H.; Albrecht, B.; Bagci, C.; Bessarab, I.; Gorska, A.; Jolic, D.; Williams, R.B.H. MEGAN-LR: New algorithms allow accurate binning and easy interactive exploration of metagenomic long reads and contigs. Biol. Direct 2018, 13, 6. [Google Scholar] [CrossRef] [PubMed]
- Langmead, B.; Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9, 357. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25, 2078–2079. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merchant, N.; Lyons, E.; Goff, S.; Vaughn, M.; Ware, D.; Micklos, D.; Antin, P. The iPlant Collaborative: Cyberinfrastructure for Enabling Data to Discovery for the Life Sciences. PLoS Biol. 2016, 14, e1002342. [Google Scholar] [CrossRef] [PubMed]
- Gallot-Lavallee, L.; Blanc, G.; Claverie, J.-M. Comparative Genomics of Chrysochromulina Ericina Virus and Other Microalga-Infecting Large DNA Viruses Highlights Their Intricate Evolutionary Relationship with the Established Mimiviridae Family. J. Virol. 2017, 91, e00230-17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Claverie, J.-M.; Abergel, C. Mimiviridae: An Expanding Family of Highly Diverse Large dsDNA Viruses Infecting a Wide Phylogenetic Range of Aquatic Eukaryotes. Viruses 2018, 10, 506. [Google Scholar] [CrossRef]
- Moniruzzaman, M.; LeCleir, G.R.; Brown, C.M.; Gobler, C.J.; Bidle, K.D.; Wilson, W.H.; Wilhelm, S.W. Genome of brown tide virus (AaV), the little giant of the Megaviridae, elucidates NCLDV genome expansion and host-virus coevolution. Virology 2014, 466, 60–70. [Google Scholar] [CrossRef]
- Yutin, N.; Colson, P.; Raoult, D.; Koonin, E.V. Mimiviridae: Clusters of orthologous genes, reconstruction of gene repertoire evolution and proposed expansion of the giant virus family. Virol. J. 2013, 10, 106. [Google Scholar] [CrossRef]
- Short, S.M.; Staniewski, M.A.; Chaban, Y.V.; Long, A.M.; Wang, D. The Diversity of Viruses Infecting Eukaryotic Algae. In Viruses of Microorganisms: Diversity, Molecular Biology and Application; Hymen, P., Abedon, S., Eds.; Caister Academic Press: Norfolk, UK, 2018; pp. 211–244. [Google Scholar]
- Wickham, H. ggplot2: Elegant Graphics for Data Analysis; Springer: New York, NY, USA, 2009. [Google Scholar]
- Oksanen, J.; Blanchet, F.G.; Friendly, M.; Kindt, R.; Legendre, P.; McGlinn, D.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; et al. Vegan: Community Ecology Package. R Package Version 2.4-5. 2017. Available online: https://CRAN.R-project.org/package=vegan (accessed on 8 October 2018).
- Schulz, F.; Yutin, N.; Ivanova, N.N.; Ortega, D.R.; Lee, T.K.; Vierheilig, J.; Daims, H.; Horn, M.; Wagner, M.; Jensen, G.J.; et al. Giant viruses with an expanded complement of translation system components. Science 2017, 356, 82–85. [Google Scholar] [CrossRef] [Green Version]
- Mokili, J.L.; Rohwer, F.; Dutilh, B.E. Metagenomics and future perspectives in virus discovery. Curr. Opin. Virol. 2012, 2, 63–77. [Google Scholar] [CrossRef]
- Forterre, P. The virocell concept and environmental microbiology. ISME J. 2013, 7, 233–236. [Google Scholar] [CrossRef] [PubMed]
- Hewson, I.; Fuhrman, J.A. Viriobenthos production and virioplankton sorptive scavenging by suspended sediment particles in coastal and pelagic waters. Microb. Ecol. 2003, 46, 337–347. [Google Scholar] [CrossRef] [PubMed]
- Templeton, M.R.; Andrews, R.C.; Hofmann, R. Particle-associated viruses in water: Impacts on disinfection processes. Crit. Rev. Environ. Sci. Technol. 2008, 38, 137–164. [Google Scholar] [CrossRef]
- Desnues, C.; Raoult, D. Inside the Lifestyle of the Virophage. Intervirology 2010, 53, 293–303. [Google Scholar] [CrossRef] [PubMed]
- Berjon-Otero, M.; Koslova, A.; Fischer, M.G. The dual lifestyle of genome-integrating virophages in protists. Ann. N. Y. Acad. Sci. 2019, 1447, 97–109. [Google Scholar] [CrossRef]
- Fischer, M.G.; Hackl, T. Host genome integration and giant virus-induced reactivation of the virophage mavirus. Nature 2016, 540, 288–291. [Google Scholar] [CrossRef] [PubMed]
- Lindgreen, S.; Adair, K.L.; Gardner, P.P. An evaluation of the accuracy and speed of metagenome analysis tools. Sci. Rep. 2016, 6, 19233. [Google Scholar] [CrossRef]
- Posedowski, B. Dundas Wastewater Treatment Plant and Cootes Paradise; City of Hamilton Public Works Department: Hamilton, ON, Canada, 2018; Available online: https://pub-hamilton.escribemeetings.com/filestream.ashx?DocumentId=150416 (accessed on 7 March 2018).
- Haffner, G.D.; Harris, G.P.; Jarai, M.K. Physical variability and phytoplankton communities 3. Vertical structure in phytoplankton populations. Arch. Hydrobiol. 1980, 89, 363–381. [Google Scholar]
- Wu, J.; Tsanis, I.K.; Chiocchio, F. Observed currents and water levels in Hamilton Harbour. J. Great Lakes Res. 1996, 22, 224–240. [Google Scholar] [CrossRef]
- Yerubandi, R.R.; Marvin, C.H.; Zhao, J. Application of a numerical model for circulation, temperature and pollutant distribution in Hamilton Harbour. J. Great Lakes Res. 2009, 35, 61–73. [Google Scholar] [CrossRef]
- Yerubandi, R.R.; Boegman, L.; Bolkhari, H.; Hiriart-Baer, V. Physical processes affecting water quality in Hamilton Harbour. Aquat. Ecosyst. Health Manag. 2016, 19, 114–123. [Google Scholar] [CrossRef]
- Munawar, M.; Fitzpatrick, M. Microbial—Planktonic foodweb dynamics of a eutrophic Area of Concern: Hamilton Harbour. Aquat. Ecosyst. Health Manag. 2017, 20, 214–229. [Google Scholar] [CrossRef]
- Munawar, M.; Fitzpatrick, M.; Niblock, H.; Kling, H.; Rozon, R.; Lorimer, J. Phytoplankton ecology of a culturally eutrophic embayment: Hamilton Harbour, Lake Ontario. Aquat. Ecosyst. Health Manag. 2017, 20, 201–213. [Google Scholar] [CrossRef]
- Saati, R. Characterization of the Cyanobacterial Harmful Algal Bloom Community in Hamilton Harbour. Master’s Thesis, University of Toronto, Toronto, ON, Canada, November 2016. [Google Scholar]
- Krupovic, M.; Koonin, E.V. Self-synthesizing transposons: Unexpected key players in the evolution of viruses and defense systems. Curr. Opin. Microbiol. 2016, 31, 25–33. [Google Scholar] [CrossRef] [PubMed]
- Claverie, J.M.; Abergel, C. Mimivirus and its Virophage. In Annual Review of Genetics; Publisher: Palo Alto, CA, USA, 2009; Volume 43, pp. 49–66. [Google Scholar]
- La Scola, B.; Desnues, C.; Pagnier, I.; Robert, C.; Barrassi, L.; Fournous, G.; Merchat, M.; Suzan-Monti, M.; Forterre, P.; Koonin, E.; et al. The virophage as a unique parasite of the giant mimivirus. Nature 2008, 455, 7218. [Google Scholar] [CrossRef] [PubMed]
- Yau, S.; Lauro, F.M.; DeMaere, M.Z.; Brown, M.V.; Thomas, T.; Raftery, M.J.; Andrews-Pfannkoch, C.; Lewis, M.; Hoffman, J.M.; Gibson, J.A.; et al. Virophage control of antarctic algal host-virus dynamics. Proc. Natl. Acad. Sci. USA 2011, 108, 6163–6168. [Google Scholar] [CrossRef]
- Koonin, E.V.; Krupovic, M. Polintons, virophages and transpovirons: A tangled web linking viruses, transposons and immunity. Curr. Opin. Virol. 2017, 25, 7–15. [Google Scholar] [CrossRef] [PubMed]
- Stough, J.M.A.; Yutin, N.; Chaban, Y.V.; Moniruzzaman, M.; Gann, E.R.; Pound, H.L.; Steffen, M.M.; Black, J.N.; Koonin, E.V.; Wilhelm, S.W.; et al. Genome and Environmental Activity of a Chrysochromulina parva Virus and Its Virophages. Front. Microbiol. 2019, 10, 703. [Google Scholar] [CrossRef]
- Fuhrman, J.A. Marine viruses and their biogeochemical and ecological effects. Nature 1999, 399, 541–548. [Google Scholar] [CrossRef]
- Suttle, C.A. Marine viruses – major players in the global ecosystem. Nat. Rev. Microbiol. 2007, 5, 801–812. [Google Scholar] [CrossRef]
- Brussard, C.P.; Wilhelm, S.W.; Thingstad, F.; Weinbauer, M.G.; Bratbak, G.; Heldal, M.; Kimmance, S.A.; Middelboe, M.; Nagasaki, K.; Paul, J.H.; et al. Global-scale processes with a nanoscale drive: The role of marine viruses. ISME J. 2008, 2, 575–578. [Google Scholar] [CrossRef] [PubMed]
- Wommack, K.E.; Colwell, R.R. Virioplankton: Viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 2000, 64, 69–114. [Google Scholar] [CrossRef]
- Liu, H.; Yuan, X.C.; Xu, J.; Harrison, P.J.; He, L.; Yin, K.D. Effects of viruses on bacterial functions under contrasting nutritional conditions for four species of bacteria isolated from Hong Kong waters. Sci. Rep. 2015, 5, 14217. [Google Scholar] [CrossRef] [PubMed]
- Wilhelm, S.W.; Suttle, C.A. Viruses and Nutrient Cycles in the Sea—Viruses play critical roles in the structure and function of aquatic food webs. Bioscience 1999, 49, 781–788. [Google Scholar] [CrossRef]
- Filee, J.; Forterre, P.; Laurent, J. The role played by viruses in the evolution of their hosts: A view based on informational protein phylogenies. Res. Microbiol. 2003, 154, 237–243. [Google Scholar] [CrossRef]
Sample | Initial DNA Concentration (ng/μL) | Library Concentration (ng/μL) | Average Library Size (bp) |
---|---|---|---|
30 July—nearshore | 5.30 | 16.2 | 985 |
30 July—mid-harbour | 2.84 | 18.3 | 1070 |
13 August—nearshore | 2.76 | 17.5 | 1070 |
13 August—mid-harbour | 3.40 | 14.5 | 1000 |
27 August—nearshore | 2.28 * | 15.0 | 950 |
27 August—mid-harbour | 1.42 * | 8.94 | 615 |
10 September—nearshore | 9.58 | 12.0 | 1000 |
10 September—mid-harbour | 10.6 | 14.1 | 1060 |
24 September—nearshore | 9.10 | 15.7 | 1030 |
24 September—mid-harbour | 2.68 | 17.7 | 900 |
Sample | Reads Pre-QC | Reads Post-QC | Contigs Post-Assembly (Mean Length; Standard Deviation; Median Length) | Contigs Assigned | Virus Contigs Assigned (Mean Length ± Standard Deviation; Median Length) | Percent of Virus Contigs |
---|---|---|---|---|---|---|
30 July—nearshore | 13,403,832 | 11,608,892 | 480,233 (692; 589; 526) | 212,156 | 349 (681; 326; 563) | 0.16 |
30 July—mid-harbour | 13,206,316 | 11,246,470 | 433,927 (823; 1540; 563) | 256,277 | 397 (626; 341; 526) | 0.15 |
13 August—nearshore | 12,758,364 | 11,040,814 | 398,774 (741; 1493; 531) | 196,128 | 488 (767; 405; 650) | 0.25 |
13 August—mid-harbour | 13,104,992 | 11,414,576 | 416,468 (820; 1060; 571) | 273,693 | 662 (688; 357; 570) | 0.24 |
27 August—nearshore | 15,685,750 | 13,953,600 | 374,464 (661; 923; 498) | 128,233 | 484 (693; 300; 592) | 0.38 |
27 August—mid-harbour | 16,101,196 | 14,751,904 | 233,868 (833; 1567; 568) | 183,817 | 232 (731; 460; 555) | 0.13 |
10 September—nearshore | 16,228,148 | 14,257,158 | 418,490 (609; 848; 487) | 110,567 | 463 (736; 327; 642) | 0.42 |
10 September—mid-harbour | 15,411,142 | 13,561,346 | 443,692 (568; 765; 474) | 64,142 | 604 (753; 320; 673) | 0.94 |
24 September—nearshore | 14,689,040 | 12,764,018 | 367,778 (629; 873; 491) | 112,144 | 372 (810; 612; 676) | 0.33 |
24 September—mid-harbour | 13,151,390 | 11,228,970 | 296,813 (776; 1094; 550) | 185,913 | 104 (870; 1257; 489) | 0.06 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Palermo, C.N.; Fulthorpe, R.R.; Saati, R.; Short, S.M. Metagenomic Analysis of Virus Diversity and Relative Abundance in a Eutrophic Freshwater Harbour. Viruses 2019, 11, 792. https://doi.org/10.3390/v11090792
Palermo CN, Fulthorpe RR, Saati R, Short SM. Metagenomic Analysis of Virus Diversity and Relative Abundance in a Eutrophic Freshwater Harbour. Viruses. 2019; 11(9):792. https://doi.org/10.3390/v11090792
Chicago/Turabian StylePalermo, Christine N., Roberta R. Fulthorpe, Rosemary Saati, and Steven M. Short. 2019. "Metagenomic Analysis of Virus Diversity and Relative Abundance in a Eutrophic Freshwater Harbour" Viruses 11, no. 9: 792. https://doi.org/10.3390/v11090792