Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AEM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Applied and Environmental Microbiology
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AEM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Environmental Microbiology

Seasonal Distribution of Cyprinid Herpesvirus 3 in Lake Biwa, Japan

Toshifumi Minamoto, Mie N. Honjo, Zen'ichiro Kawabata
Toshifumi Minamoto
Research Institute for Humanity and Nature, 457-4 Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: minamoto@chikyu.ac.jp
Mie N. Honjo
Research Institute for Humanity and Nature, 457-4 Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Zen'ichiro Kawabata
Research Institute for Humanity and Nature, 457-4 Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/AEM.01411-09
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

The seasonal distribution of the cyprinid herpesvirus 3 (CyHV-3) in Lake Biwa, Japan, was investigated. CyHV-3 was distributed all over the lake 5 years after the first outbreak. The mean concentration of CyHV-3 in water showed annual oscillation, with a peak in the summer and a trough in winter. Our results suggested that CyHV-3 is present at high density in reductive environments, such as reed zones and turbid or eutrophic water.

A novel fatal disease of fish caused by cyprinid herpesvirus 3 (CyHV-3), also known as koi herpesvirus or carp interstitial nephritis and gill necrosis virus, which infects the common carp (Cyprinus carpio carpio) and ornamental koi (Cyprinus carpio koi) was reported at the end of the 1990s, and it has spread rapidly worldwide (13). In 2003, the first mass mortality in Japan was observed in Lake Kasumigaura, Ibaraki Prefecture (17), and the disease immediately spread all over the country.

Lake Biwa is the largest and oldest freshwater lake in Japan. It occupies 670 km2, and the total length of the coastline is 241 km. The first and relatively small-scale mortality caused by CyHV-3 was observed in the autumn of 2003 in Lake Biwa, and mass mortality occurred in the following spring, in which more than 100,000 carp died (10). Thus, the disease is a great threat not only to the cultivation industry and koi collectors but also to the natural carp population. Carp is regarded as an ecological engineer that has an impact on freshwater ecosystems, and therefore, mass mortality will affect the entire lake ecosystem (10).

The pathogenesis and diagnosis of the disease have been studied intensively, but the dynamics of CyHV-3 has not been clarified. Recently, the major portal of CyHV-3 entry was reported to be fish skin (2), which means that infection via water is possible. Thus, to determine the method by which the virus spreads and to evaluate the infectious risk in the environment, one must clarify the CyHV-3 dynamics in the natural environment. In the present study, we surveyed the seasonal distribution pattern of CyHV-3 in Lake Biwa, Japan, using a quantitative method.

Concentration and quantification of viruses in environmental water.

Twenty-two sampling sites were selected on the coastline of Lake Biwa, Japan (Fig. 1A) (see Table S1 in the supplemental material). Four liters of the lake surface water was collected in plastic tanks from these sites in 2007 in May to July, August, and November and in 2008 in February, May, June, August, October, and December (see Table S2 in the supplemental material). Although the first sampling was carried out from 15 May to 2 July 2007, hereafter, for simplicity, we refer to these as June 2007 samples. The water samples in plastic tanks were transported to the laboratory at room temperature. It took about 3 hours on average for transportation, and then the samples were stored at 4°C. To count the total number of viruslike particles and bacteria, 10-ml water samples were fixed with 2% formaldehyde and kept at 4°C. Samples were filtered onto 0.02-μm-pore-size Anodisc filters (Whatman) and stained with SYBR green I (Molecular Probes), and the enumeration of viruslike particles and bacteria was performed directly using an epifluorescence microscope (12). The other water quality parameters were measured on-site (Table 1) (see Table S2 in the supplemental material).

FIG. 1.
  • Open in new tab
  • Download powerpoint
FIG. 1.

(A) Study sites. The lake surface water was collected at 22 sites (sites a to v) on the coastline. The sampling sites are indicated by closed circles. (B) Seasonal distribution of CyHV-3 in Lake Biwa, Japan. Lake surface water was collected from 22 sites on nine occasions from June 2007 to December 2008. We calculated the CyHV-3 concentration (number of copies per liter) only when all three replicate samples showed positive results, and data were treated as “under the quantification limit” when only one or two positive results were obtained. Abbreviations: Jun, June; Aug, August; Nov, November; Feb, February; Oct, October; Dec, December.

View this table:
  • View inline
  • View popup
TABLE 1.

Characteristics of water samples from Lake Biwa, Japan

Virus concentration was performed on the next day of water sampling via a modified version of the cation-coated filter method (11; M. N. Honjo, T. Minamoto, K. Matsui, K. Uchii, H. Yamanaka, A. A. Suzuki, Y. Kohmatsu, T. Iida, and Z. Kawabata, submitted for publication). In brief, to estimate the CyHV-3 concentration, a known amount (1 × 107 viruslike particles liter−1) of lambda phage was added to each water sample as an external standard. Viruses in the prefiltered lake water (4 liters) were trapped with cation (Al3+)-coated 0.45-μm HA electronegative filters (HAWP14250; Millipore, Japan). After the viruses were rinsed with 0.5 mM H2SO4, they were eluted with 200 ml of 1.0 mM NaOH. The concentrated viruses were then precipitated with 8% polyethylene glycol 6000 and 0.4 M NaCl at 4°C overnight and then centrifuged at 10,000 × g for 1 h. Viral DNA was extracted and purified by the phenol-chloroform method (16) and then further purified with the DNeasy blood and tissue kit (Qiagen, Germany). The final volume of the DNA solution was 100 μl. CyHV-3 and lambda DNA was quantified with a real-time TaqMan PCR (5; Honjo et al., submitted) using StepOnePlus real-time PCR systems (Applied Biosystems). For virus quantification, 5 μl and 2 μl of DNA solution were used as templates for CyHV-3 and lambda measurements, respectively, and the total volume of each reaction mixture was 20 μl. Three replicates were performed for each set.

The mean recovery yield of the lambda was 12.6% for all samples. Given that the recovery rate of CyHV-3 versus that of lambda is 0.71 (Honjo et al., submitted), the mean CyHV-3 recovery yield was estimated as 8.9%, which was higher than that in a recent study (1.6%) in which the cation-coated filter method was adopted (7). Although our method is fundamentally the same as theirs, more elution fluid (4.4 times per area) was used in our study, which might be the reason for the higher recovery yields in the present study. Combining the estimated recovery yields and the quantification limit of real-time PCR (three copies per tube) (Honjo et al., submitted) revealed that the mean limit of our method was 170 copies liter−1. Considering the results described below, our method is useful for quantifying CyHV-3 in the late spring, summer, and autumn when the CyHV-3 concentration is relatively high; however, further modification of the method with a higher recovery yield and/or greater water capacity is required in winter or early spring.

CyHV-3 distribution in Lake Biwa.

CyHV-3 DNA was distributed all over the lake, even in winter (Fig. 1B). The mean concentration of CyHV-3 in water showed an annual oscillation with a peak in the summer and a trough in winter (Fig. 2). In Lake Biwa, relatively small numbers of dead carp infected with CyHV-3 have been found every year after the mass mortality in 2004 (Shiga Prefectural Fisheries Experiment Station, unpublished data). Such seasonal fluctuation in CyHV-3 concentration may have continued for years after the first outbreak in Lake Biwa. Most adult carp show a relatively high CyHV-3 antibody level, which indicates past infection history (19). Generally herpesviruses that infect fishes show latent infection and reactivation (6, 14). Although CyHV-3 latency has not been confirmed, it is assumed that CyHV-3 also shows this feature (18). Accordingly, surviving fish become carriers that release the virus in the warm season and produce new infections and carriers. Thus, chronic presentation of CyHV-3 in Lake Biwa is conceivable. More generally, once CyHV-3 has invaded an aquatic environment, it will remain for a substantial period of time.

FIG. 2.
  • Open in new tab
  • Download powerpoint
FIG. 2.

Seasonal changes in mean CyHV-3 concentration. “Under quantification limit” and “not detected” were treated as 0. The mean concentration (number of copies per liter) of CyHV-3 in the water showed an annual oscillation, with a peak in August and a trough in February. Abbreviations: conc., concentration; Apr.07, April 2007; Jun.07, June 2007; Aug.07, August 2007; Oct.07, October 2007; Dec.07, December 2007; Feb.08, February 2008.

Most dead fish infected with CyHV-3 are found in late spring (June to July) and autumn (November to December) in Lake Biwa, Japan, and few are found in the summer. Since the temperature range of 18 to 25°C is required for disease development (15), such a pattern of infected fish detection is accepted as reasonable. However, the present study showed that the estimated CyHV-3 concentration is highest in August (Fig. 2). The reason for this discrepancy is unclear, but the activity of CyHV-3 might not be completely inert at such a high nonpermissive temperature (3). Further study is required to clarify this point.

A long-term question has been how CyHV-3 survives the winter season. Haramoto et al. (8) have reported the detection of CyHV-3 DNA from a river in winter. We also showed the presence of CyHV-3 DNA even in February when the water temperature falls below 10°C (Fig. 1B). These results suggest that the virus carriers release CyHV-3 even in winter when viral activity is predicted to be at its lowest. Given that carp and koi are the only natural hosts of the virus, CyHV-3 is predicted to retain its activity at nonpermissive low temperatures and the virus is released continuously from carp, even at a low level in the winter. Alternatively, CyHV-3 might survive the winter season in the lake sediment, and a small amount of virus may become detached from the sediment and appear in the surface water. This hypothesis is realistic, because active virus can be detected from carp droppings under experimental conditions (4). In this case, the bottom-feeding behavior of carp might be involved in spreading the virus/disease.

Correlation between CyHV-3 concentration and water quality.

Although the detection of virus DNA does not directly mean the presence of active virus, understanding where the virus is present at high density is important to evaluate the risk of CyHV-3 disease as well as to clarify the ecology of the virus. We investigated the relationships between the CyHV-3 concentration and each water quality parameter obtained. The log CyHV-3 concentration showed a significant positive correlation with water temperature, turbidity, chlorophyll a concentration, and total bacterial count (Pearson correlation coefficients [r] = 0.31, 0.24, 0.26, and 0.19, respectively), and showed a significant negative correlation with the oxidation reduction potential (ORP) (r = −0.39) (Fig. 3) (see Table S3 in the supplemental material). Among these factors, the strongest correlation was that with the ORP. The result showed that more CyHV-3 particles are present at lower ORP sites, i.e., more reductive environments. This result supports the hypothesis that spawning sites are one source of infection (19), because the reed zones, the main spawning sites of carp in Lake Biwa, are generally muddy and reductive environments (9). In the highly turbid water, viruses may escape predation or degradation by attaching to organic or nonorganic particles. The chlorophyll concentration and the total bacterial count are indicators of eutrophication, and therefore, our results suggest that the CyHV-3 concentration increases in nutrient-rich sites. However, the mechanism involved remains unclear.

FIG. 3.
  • Open in new tab
  • Download powerpoint
FIG. 3.

Relationships between log CyHV-3 concentration and each water quality parameter. Only parameters with significant correlations are shown. (A to D) Water temperature, turbidity, chlorophyll concentration, and total numbers of bacterium-like particles showed a significant positive correlation with log CyHV-3 concentration (number of copies per liter) (r = 0.31, 0.24, 0.26, and 0.19, respectively). (E) ORP showed a significant negative correlation (r = −0.39). Regression lines are also shown. Abbreviations: Conc., concentration; NTU, nephelometric turbidity units.

Sequence comparisons with published genomes.

Forty liters of lake surface water was collected at site q on 1 October 2008, and the viral DNA was collected and purified as described above. Genomic DNA fragments in which insertions/deletions (indels) and/or substitutions were observed among three published CyHV-3 genomes (1) were amplified with newly designed primer sets (Table 2), and amplified fragments were directly sequenced. The DDBJ accession numbers for these fragments are AB505896 to AB505901. In an examination of the 2,399-bp sequence, the sequence of the Lake Biwa CyHV-3 genome matched completely that of the reported Japanese strain. Previously we sequenced CyHV-3 fragments obtained from Yura River, Japan, and the sequence also matched that of the Japanese strain (11). These results suggest that CyHV-3 obtained from Japanese environmental waters shares the same origins with the virus that caused mass mortality.

View this table:
  • View inline
  • View popup
TABLE 2.

Detailed information on the PCR-amplified region for sequences

In this study, we demonstrated the seasonal distribution of CyHV-3 in Lake Biwa, Japan, though we cannot show the viral activity. To the best of our knowledge, this is the first report to show viral distribution patterns across seasons in the natural environment. Although the increasing/decreasing pattern did not coincide with the detection pattern of the infected fish, it gives new insight into our knowledge of CyHV-3 dynamics. Our results showed that CyHV-3 has remained for at least 5 years from the first outbreak, with seasonal fluctuation, which suggests the development of CyHV-3 in Lake Biwa. Understanding the ecology of CyHV-3 in natural environments may be useful in preventing the spread of CyHV-3.

ACKNOWLEDGMENTS

We thank Tomoaki Itayama and Nobuyuki Tanaka (Research Institute of Environmental Eco-Technology, Japan) for helpful discussions about the virus concentration methods.

This work was supported by the Research Institute for Humanity and Nature (RIHN) C-06 research project and a Grant-in-Aid for Young Scientists (B: 20710013) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

FOOTNOTES

    • Received 17 June 2009.
    • Accepted 24 August 2009.
  • Copyright © 2009 American Society for Microbiology

REFERENCES

  1. 1.↵
    Aoki, T., I. Hirono, K. Kurokawa, H. Fukuda, R. Nahary, A. Eldar, A. J. Davison, T. B. Waltzek, H. Bercovier, and R. P. Hedrick. 2007. Genome sequences of three koi herpesvirus isolates representing the expanding distribution of an emerging disease threatening koi and common carp worldwide. J. Virol.81:5058-5065.
    OpenUrlAbstract/FREE Full Text
  2. 2.↵
    Costes, B., V. Stalin Raj, B. Michel, G. Fournier, M. Thirion, L. Gillet, J. Mast, F. Lieffrig, M. Bremont, and A. Vanderplasschen. 19 January 2009. The major portal of entry of koi herpesvirus in Cyprinus carpio is the skin. J. Virol. doi:10.1128/JVI.02305-08.
    OpenUrlAbstract/FREE Full Text
  3. 3.↵
    Dishon, A., M. Davidovich, M. Ilouze, and M. Kotler. 2007. Persistence of cyprinid herpesvirus 3 in infected cultured carp cells. J. Virol.81:4828-4836.
    OpenUrlAbstract/FREE Full Text
  4. 4.↵
    Dishon, A., A. Perelberg, J. Bishara-Shieban, M. Ilouze, M. Davidovich, S. Werker, and M. Kotler. 2005. Detection of carp interstitial nephritis and gill necrosis virus in fish droppings. Appl. Environ. Microbiol.71:7285-7291.
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    Gilad, O., S. Yun, F. J. Zagmutt-Vergara, C. M. Leutenegger, H. Bercovier, and R. P. Hedrick. 2004. Concentrations of a koi herpesvirus (KHV) in tissues of experimentally infected Cyprinus carpio koi as assessed by real-time TaqMan PCR. Dis. Aquat. Organ.60:179-187.
    OpenUrlCrossRefPubMed
  6. 6.↵
    Gray, W. L., R. J. Williams, R. L. Jordan, and B. R. Griffin. 1999. Detection of channel catfish virus DNA in latently infected catfish. J. Gen. Virol.80:1817-1822.
    OpenUrlPubMedWeb of Science
  7. 7.↵
    Haramoto, E., M. Kitajima, H. Katayama, T. Ito, and S. Ohgaki. 2009. Development of virus concentration methods for detection of koi herpesvirus in water. J. Fish Dis.32:297-300.
    OpenUrlCrossRefPubMed
  8. 8.↵
    Haramoto, E., M. Kitajima, H. Katayama, and S. Ohgaki. 2007. Detection of koi herpesvirus DNA in river water in Japan. J. Fish Dis.30:59-61.
    OpenUrlPubMedWeb of Science
  9. 9.↵
    Karube, Z., N. Okada, and I. Tayasu. 2008. Food web in reed zone around Lake Biwa: analysis from carbon, nitrogen and sulfur stable isotope ratio, p. 354. In Proceedings of the 55th Annual Meeting of the Ecological Society of Japan. The Ecological Society of Japan, Kyoto, Japan. (In Japanese.)
  10. 10.↵
    Matsui, K., M. Honjo, Y. Kohmatsu, K. Uchii, R. Yonekura, and Z. Kawabata. 2008. Detection and significance of koi herpesvirus (KHV) in freshwater environments. Freshwater Biol.53:1262-1272.
    OpenUrlCrossRef
  11. 11.↵
    Minamoto, T., M. N. Honjo, K. Uchii, H. Yamanaka, A. A. Suzuki, Y. Kohmatsu, T. Iida, and Z. Kawabata. 2009. Detection of cyprinid herpesvirus 3 DNA in river water during and after an outbreak. Vet. Microbiol.135:261-266.
    OpenUrlCrossRefPubMed
  12. 12.↵
    Noble, R. T., and J. A. Fuhrman. 1998. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol.14:113-118.
    OpenUrlCrossRef
  13. 13.↵
    Pokorova, D., T. Vesely, V. Piackova, S. Reschova, and J. Hulova. 2005. Current knowledge on koi herpesvirus (KHV): a review. Vet. Med. Czech.50:139-147.
    OpenUrl
  14. 14.↵
    Rijsewijk, F., S. Pritz-Verschuren, S. Kerkhoff, A. Botter, M. Willemsen, T. V. Nieuwstadt, and O. Haenen. 2005. Development of a polymerase chain reaction for the detection of anguillid herpesvirus DNA in eels based on the herpesvirus DNA polymerase gene. J. Virol. Methods124:87-94.
    OpenUrlCrossRefPubMed
  15. 15.↵
    Ronen, A., A. Perelberg, J. Abramowitz, M. Hutoran, S. Tinman, I. Bejerano, M. Steinitz, and M. Kotler. 2003. Efficient vaccine against the virus causing a lethal disease in cultured Cyprinus carpio. Vaccine21:4677-4684.
    OpenUrlCrossRefPubMed
  16. 16.↵
    Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  17. 17.↵
    Sano, M., T. Ito, J. Kurita, T. Yanai, N. Watanabe, S. Miwa, and T. Iida. 2004. First detection of koi herpesvirus in cultured common carp Cyprinus carpio in Japan. Fish Pathol.39:165-167.
    OpenUrl
  18. 18.↵
    St-Hilaire, S., N. Beevers, K. Way, R. M. Le Deuff, P. Martin, and C. Joiner. 2005. Reactivation of koi herpesvirus infections in common carp Cyprinus carpio. Dis. Aquat. Organ.67:15-23.
    OpenUrlCrossRefPubMed
  19. 19.↵
    Uchii, K., K. Matsui, T. Iida, and Z. Kawabata. 4 June 2009. Distribution of the introduced cyprinid herpesvirus 3 in a wild population of common carp, Cyprinus carpio. J. Fish Dis. doi:10.1111/j.1365-2761.2009.01064.x.
    OpenUrlCrossRef
PreviousNext
Back to top
Download PDF
Citation Tools
Seasonal Distribution of Cyprinid Herpesvirus 3 in Lake Biwa, Japan
Toshifumi Minamoto, Mie N. Honjo, Zen'ichiro Kawabata
Applied and Environmental Microbiology Oct 2009, 75 (21) 6900-6904; DOI: 10.1128/AEM.01411-09

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Applied and Environmental Microbiology article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Seasonal Distribution of Cyprinid Herpesvirus 3 in Lake Biwa, Japan
(Your Name) has forwarded a page to you from Applied and Environmental Microbiology
(Your Name) thought you would be interested in this article in Applied and Environmental Microbiology.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Seasonal Distribution of Cyprinid Herpesvirus 3 in Lake Biwa, Japan
Toshifumi Minamoto, Mie N. Honjo, Zen'ichiro Kawabata
Applied and Environmental Microbiology Oct 2009, 75 (21) 6900-6904; DOI: 10.1128/AEM.01411-09
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • Concentration and quantification of viruses in environmental water.
    • CyHV-3 distribution in Lake Biwa.
    • Correlation between CyHV-3 concentration and water quality.
    • Sequence comparisons with published genomes.
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

Fresh Water
Herpesviridae
Seasons

Related Articles

Cited By...

About

  • About AEM
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #AppEnvMicro

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

 

Print ISSN: 0099-2240; Online ISSN: 1098-5336