Skip to main content
SpringerLink
Log in

Morphological Characterization of Viruses in the Stratified Water Column of Alkaline, Hypersaline Mono Lake

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Concentrations of viruses and prokaryotes in the alkaline, moderately hypersaline, seasonally stratified Mono Lake are among the highest reported for a natural aquatic environment. We used electron microscopy to test whether viral morphological characteristics differed among the epilimnion, metalimnion, and the anoxic hypolimnion of the lake and to determine how the properties of viruses in Mono Lake compare to other aquatic environments. Viral capsid size distributions were more similar in the metalimnion and hypolimnion of Mono Lake, while viral tail lengths were more similar in the epilimnion and metalimnion. The percentage of tailed viruses decreased with depth and the relative percentages of tailed phage families changed with depth. The presence of large (>125 nm capsid), untailed viruses in the metalimnion and hypolimnion suggests that eukaryotic viruses are produced in these suboxic and anoxic, hypersaline environments. Capsid diameters of viruses were larger on average in Mono Lake compared to other aquatic environments, and no lemon-shaped or filamentous viruses were found, in contrast to other high-salinity or high-altitude lakes and seas. Our data suggest that the physically and chemically distinct layers of Mono Lake harbor different viral assemblages, and that these assemblages are distinct from other aquatic environments that have been studied. Furthermore, we found that filtration of a sample through a 0.22-µm pore-size filter significantly altered the distribution of viral capsid diameters and tail lengths, resulting in a relative depletion of viruses having larger capsids and longer tails. This observation highlights the potential for bias in molecular surveys of viral diversity, which typically rely on filtration through 0.2- or 0.22-µm pore-size membrane filters to remove bacteria during sample preparation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Bench SR, Hanson TE, Williamson KE, Ghosh D, Radosovich M, Wang K, Wommack KE (2007) Metagenomic characterization of Chesapeake Bay virioplankton. Appl Environ Microbiol 73:7629–7641

    Article  CAS  PubMed  Google Scholar 

  2. Bettarel Y, Amblard C, Sime-Ngando T, Carrias J-F, Sargos D, Garabetian F, Lavandier P (2003) Viral lysis, flagellate grazing potential, and bacterial production in Lake Pavin. Microb Ecol 45:119–127

    Article  CAS  PubMed  Google Scholar 

  3. Boehrer B, Schultze M (2008) Stratification of lakes. Reviews of Geophysics 46:RG2005

  4. Bratbak G, Haslund OH, Heldal M, Naess A, Roeggen T (1992) Giant marine viruses? Mar Ecol Prog Ser 85:202–202

    Article  Google Scholar 

  5. Breitbart M, Felts B, Kelley S, Mahaffy JM, Nulton J, Salamon P, Rohwer F (2004) Diversity and population structure of a near-shore marine-sediment viral community. Proc R Soc B 271:565–574

    Article  PubMed  Google Scholar 

  6. Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, Azam F, Rohwer F (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99:14250–14255

    Article  CAS  PubMed  Google Scholar 

  7. Brum JR, Steward GF, Jiang SC, Jellison R (2005) Spatial and temporal variability of prokaryotes, viruses, and viral infections of prokaryotes in an alkaline, hypersaline lake. Aquat Microb Ecol 41:247–260

    Article  Google Scholar 

  8. Castberg T, Thyrhaug R, Larsen A, Sandaa R-A, Heldal M, Van Etten JL, Bratbak G (2002) Isolation and characterization of a virus that infects Emiliania huxleyi (Haptophyta). J Phycol 38:767–774

    Article  CAS  Google Scholar 

  9. Colombet J, Robin A, Lavie L, Bettarel Y, Cauchie HM, Sime-Ngando T (2007) Virioplankton 'pegylation': Use of PEG (polyethylene glycol) to concentrate and purify viruses in pelagic ecosystems. J Microbiol Meth 71:212–219

    Article  CAS  Google Scholar 

  10. Colombet J, Sime-Ngando T, Cauchie HM, Fonty G, Hoffmann L, Demeure G (2006) Depth-related gradients of viral activity in Lake Pavin. Appl Environ Microbiol 72:4440–4445

    Article  CAS  PubMed  Google Scholar 

  11. Culley AI, Lang AS, Suttle CA (2006) Metagenomic analysis of coastal RNA virus communities. Science 312:1795–1798

    Article  CAS  PubMed  Google Scholar 

  12. Davidson LA, Davidson AE (2005) The range of protists in Mono Lake, a hypersaline soda lake in the eastern sierras. J Eukaryot Microbiol 52:11S

    Article  Google Scholar 

  13. Demuth J, Neve H, Witzel K-P (1993) Direct electron microscopy study on the morphological diversity of bacteriophage populations in Lake Plussee. Appl Environ Microbiol 59:3378–3384

    CAS  PubMed  Google Scholar 

  14. Edgcomb V, Orsi W, Leslin C, Epstein SS, Bunge J, Jeon S, Yakimov MM, Behnke A, Stoeck T (2009) Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the eastern Mediterranean Sea. Extremophiles 13:151–167

    Article  PubMed  Google Scholar 

  15. Finlay BJ (1990) Physiological ecology of free-living protozoa. Adv Microb Ecol 11:1–34

    CAS  Google Scholar 

  16. Garza DR, Suttle CA (1995) Large double-stranded DNA viruses which cause the lysis of a marine heterotrophic nanoflagellate (Bodo sp) occur in natural marine viral communities. Aquat Microb Ecol 9:203–210

    Article  Google Scholar 

  17. Guixa-Boixereu N, Calderon-Paz JI, Heldal M, Bratbak G, Pedro-Alio C (1996) Viral lysis and bacteriovory as prokaryotic loss factors along a salinity gradient. Aquat Microb Ecol 11:215–227

    Article  Google Scholar 

  18. Hofer JS, Sommaruga R (2001) Seasonal dynamics of viruses in an alpine lake: importance of filamentous forms. Aquat Microb Ecol 26:1–11

    Article  Google Scholar 

  19. Hollibaugh JT, Wong PS, Bano N, Pak SK, Prager EM, Orrego C (2001) Stratification of microbial assemblages in Mono Lake, California, and response to a mixing event. Hydrobiologia 466:45–60

    Article  CAS  Google Scholar 

  20. Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69:1030–1042

    Article  CAS  PubMed  Google Scholar 

  21. Jellison R, Melack JM (1993) Algal photosynthetic activity and its response to meromixis in hypersaline Mono Lake, California. Limnol Oceanogr 38:818–837

    Article  CAS  Google Scholar 

  22. Jellison R, Melack JM (1993) Meromixis in hypersaline Mono Lake, California. 1. Stratification and vertical mixing during the onset, persistence, and breakdown of meromixis. Limnol Oceanogr 38:1008–1019

    Article  CAS  Google Scholar 

  23. Jellison R, Melack JM (2001) Nitrogen limitation and particulate elemental ratios of seston in hypersaline Mono Lake, California, U.S.A. Hydrobiologia 466:1–12

    Article  CAS  Google Scholar 

  24. Jellison R, Melack JM (1988) Photosynthetic activity of phytoplankton and its relation to environmental factors in hypersaline Mono Lake, California. Hydrobiologia 158:69–88

    Article  CAS  Google Scholar 

  25. Jellison R, Miller LG, Melack JM, Dana GL (1993) Meromixis in hypersaline Mono Lake, California. 2. Nitrogen fluxes. Limnol Oceanogr 38:1020–1039

    Article  CAS  Google Scholar 

  26. Jellison R, Romero J, Melack JM (1998) The onset of meromixis during restoration of Mono Lake, California: unintended consequences of reducing water diversions. Limnol Oceanogr 43:706–711

    Article  Google Scholar 

  27. Jiang S, Steward G, Jellison R, Chu W, Choi S (2004) Abundance, distribution, and diversity of viruses in alkaline, hypersaline Mono Lake, California. Microb Ecol 47:9–17

    Article  CAS  PubMed  Google Scholar 

  28. Jones BE, Grant WD, Duckworth AW, Owenson GG (1998) Microbial diversity of soda lakes. Extremophiles 2:191–200

    Article  CAS  PubMed  Google Scholar 

  29. Krebs CJ (1999) Ecological Methodology, 2nd edn. Addison-Welsey Educational Publishers, Inc., Menlo Park

    Google Scholar 

  30. Lawrence JG, Hatfull GF, Hendrix RW (2002) Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 184:4891–4905

    Article  CAS  PubMed  Google Scholar 

  31. Melack JM, Jellison R (1998) Limnological conditions in Mono Lake: contrasting monomixis and meromixis in the 1990 s. Hydrobiologia 384:21–39

    Article  Google Scholar 

  32. Noble RT, Fuhrman JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14:113–118

    Article  Google Scholar 

  33. Oren A, Bratbak G, Heldal M (1997) Occurrence of virus-like particles in the Dead Sea. Extremophiles 1:143–149

    Article  CAS  PubMed  Google Scholar 

  34. Paul JH, Jiang SC, Rose JB (1991) Concentration of viruses and dissolved DNA from aquatic environments by vortex flow filtration. Appl Environ Microbiol 57:2197–2204

    CAS  PubMed  Google Scholar 

  35. Pina S, Creus A, Gonzalez N, Girones R, Felip M, Sommaruga R (1998) Abundance, morphology and distribution of planktonic virus-like particles in two high mountain lakes. J Plankton Res 20:2413–2421

    Article  Google Scholar 

  36. Reisser W (1993) Viruses and virus-like particles of freshwater and marine eukaryotic algae - a review. Archiv fur Protisten Kunde 143:257–265

    Google Scholar 

  37. Roesler CS, Culbertson CW, Etheridge SM, Goericke R, Kiene RP, Miller LG, Oremland RS (2002) Distribution, production, and ecophysiology of Picocystis strain ML in Mono Lake, California. Limnol Oceanogr 47:440–452

    Article  CAS  Google Scholar 

  38. Setala O (1991) Ciliates in the anoxic deep-water layer of the Baltic. Arch Hydrobiol 122:483–492

    Google Scholar 

  39. Sheldon RW, Sutcliffe WHJ (1969) Retention of marine particles by screens and filters. Limnol Oceanogr 14:441–444

    Article  Google Scholar 

  40. Stopar D, Cerne A, Zigman M, Poljsak-Prijatelj M, Turk V (2003) Viral abundance and a high proportion of lysogens suggests that viruses are important members of the microbial community in the Gulf of Trieste. Microb Ecol 46:249–256

    Article  CAS  PubMed  Google Scholar 

  41. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Fisheries Research Board of Canada Bulletin:167

  42. Suttle CA (2005) Viruses in the sea. Nature 437:356–361

    Article  CAS  PubMed  Google Scholar 

  43. Van Etten JL, Lane LC, Meints RH (1991) Viruses and viruslike particles of eukaryotic algae. Microbiol Rev 55:586–620

    PubMed  Google Scholar 

  44. Walker KF, Williams WD, Hammer UT (1970) The Miller method for oxygen determination applied to saline lakes. Limnol Oceanogr 15:814–815

    Article  CAS  Google Scholar 

  45. Weinbauer MG, Hofle MG (1998) Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Appl Environ Microbiol 64:431–438

    CAS  PubMed  Google Scholar 

  46. Weinbauer MG, Peduzzi P (1994) Frequency, size and distribution of bacteriophages in different marine bacterial morphotypes. Mar Ecol Prog Ser 108:11–20

    Article  Google Scholar 

  47. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114

    Article  CAS  PubMed  Google Scholar 

  48. Zar J (1996) Biostatistical Analysis, 3rd edn. Prentice Hall, Upper Saddle River

    Google Scholar 

Download references

Acknowledgements

This research was supported by grants from the US National Science Foundation (DEB 01-29174, OCE 04-42664, EF 04-24599). We thank Robert Jellison for providing logistical support in the field, hydrographic data, and review of this manuscript. We further acknowledge the logistical support provided by the Sierra Nevada Aquatic Research Laboratory through the University of California Natural Reserve System. We thank Tina Carvalho of the University of Hawai‘i Biological Electron Microscope Facility for her assistance with TEM. We also thank David Karl for reviewing and providing comments on a draft of this manuscript.

Author information

Authors and Affiliations

  1. Department of Oceanography, University of Hawai‘i at Manoa, 1000 Pope Rd., MSB 205, Honolulu, HI, 96822, USA

    Jennifer R. Brum & Grieg F. Steward

Authors
  1. Jennifer R. Brum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Grieg F. Steward
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer R. Brum.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brum, J.R., Steward, G.F. Morphological Characterization of Viruses in the Stratified Water Column of Alkaline, Hypersaline Mono Lake. Microb Ecol 60, 636–643 (2010). https://doi.org/10.1007/s00248-010-9688-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-010-9688-4

Keywords

Search

Navigation