skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer

Abstract

Viruses are the most abundant biological entity on Earth and their interactions with microbial communities are recognized to influence microbial ecology and impact biogeochemical cycling in various ecosystems. While the factors that control the distribution of viruses in surface aquatic environments are well-characterized, the abundance and distribution of continental subsurface viruses with respect to microbial abundance and biogeochemical parameters have not yet been established. In order to begin to understand the factors governing virus distribution in subsurface environments, we assessed microbial cell and virus abundance in groundwater concurrent with groundwater chemistry in a uranium impacted alluvial aquifer adjoining the Colorado River near Rifle, CO. Virus abundance ranged from 8.0 × 10 4 to 1.0 × 10 6 mL -1 and exceeded cell abundance in all samples (cell abundance ranged from 5.8 × 10 4 to 6.1 × 10 5 mL -1). The virus to microbial cell ratio ranged from 1.1 to 8.1 and averaged 3.0 ± 1.6 with virus abundance most strongly correlated to cell abundance (Spearman's ρ = 0.73, p < 0.001). Both viruses and cells were positively correlated to dissolved organic carbon (DOC) with cells having a slightly stronger correlation (Spearman's ρ = 0.46, p < 0.05 andmore » ρ = 0.54, p < 0.05; respectively). Groundwater uranium was also strongly correlated with DOC and virus and cell abundance (Spearman's ρ = 0.62, p < 0.05; ρ = 0.46, p < 0.05; and ρ = 0.50, p < 0.05; respectively). Together the data indicate that microbial cell and virus abundance are correlated to the geochemical conditions in the aquifer. As such local geochemical conditions likely control microbial host cell abundance which in turn controls viral abundance. Given the potential impacts of viral-mediated cell lysis such as liberation of labile organic matter from lysed cells and changes in microbial community structure, viral interactions with the microbiota should be considered in an effort to understand subsurface biogeochemical cycling and contaminant mobility.« less

Authors:
 [1];  [2];  [3];  [3];  [2]
  1. Univ. of Nebraska, Lincoln, NE (United States); Japan Agency for Marine-Earth Science and Technology, Yokosuka (Japan)
  2. Univ. of Nebraska, Lincoln, NE (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1398999
DOE Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal Issue: JUL; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; virus; bacteriophage; dissolved organic carbon; aquifer; subsurface; uranium; groundwater

Citation Formats

Pan, Donald, Nolan, Jason, Williams, Kenneth H., Robbins, Mark J., and Weber, Karrie A. Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01199.
Pan, Donald, Nolan, Jason, Williams, Kenneth H., Robbins, Mark J., & Weber, Karrie A. Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer. United States. doi:10.3389/fmicb.2017.01199.
Pan, Donald, Nolan, Jason, Williams, Kenneth H., Robbins, Mark J., and Weber, Karrie A. Tue . "Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer". United States. doi:10.3389/fmicb.2017.01199. https://www.osti.gov/servlets/purl/1398999.
@article{osti_1398999,
title = {Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer},
author = {Pan, Donald and Nolan, Jason and Williams, Kenneth H. and Robbins, Mark J. and Weber, Karrie A.},
abstractNote = {Viruses are the most abundant biological entity on Earth and their interactions with microbial communities are recognized to influence microbial ecology and impact biogeochemical cycling in various ecosystems. While the factors that control the distribution of viruses in surface aquatic environments are well-characterized, the abundance and distribution of continental subsurface viruses with respect to microbial abundance and biogeochemical parameters have not yet been established. In order to begin to understand the factors governing virus distribution in subsurface environments, we assessed microbial cell and virus abundance in groundwater concurrent with groundwater chemistry in a uranium impacted alluvial aquifer adjoining the Colorado River near Rifle, CO. Virus abundance ranged from 8.0 × 104 to 1.0 × 106 mL-1 and exceeded cell abundance in all samples (cell abundance ranged from 5.8 × 104 to 6.1 × 105 mL-1). The virus to microbial cell ratio ranged from 1.1 to 8.1 and averaged 3.0 ± 1.6 with virus abundance most strongly correlated to cell abundance (Spearman's ρ = 0.73, p < 0.001). Both viruses and cells were positively correlated to dissolved organic carbon (DOC) with cells having a slightly stronger correlation (Spearman's ρ = 0.46, p < 0.05 and ρ = 0.54, p < 0.05; respectively). Groundwater uranium was also strongly correlated with DOC and virus and cell abundance (Spearman's ρ = 0.62, p < 0.05; ρ = 0.46, p < 0.05; and ρ = 0.50, p < 0.05; respectively). Together the data indicate that microbial cell and virus abundance are correlated to the geochemical conditions in the aquifer. As such local geochemical conditions likely control microbial host cell abundance which in turn controls viral abundance. Given the potential impacts of viral-mediated cell lysis such as liberation of labile organic matter from lysed cells and changes in microbial community structure, viral interactions with the microbiota should be considered in an effort to understand subsurface biogeochemical cycling and contaminant mobility.},
doi = {10.3389/fmicb.2017.01199},
journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = JUL,
volume = 8,
place = {United States},
year = {2017},
month = {7}
}

Works referenced in this record:

Evidence that viral abundance across oceans and lakes is driven by different biological factors
journal, June 2008


Ocean viruses and their effects on microbial communities and biogeochemical cycles
journal, September 2012

  • Weitz, Joshua; Wilhelm, Steven
  • F1000 Biology Reports
  • DOI: 10.3410/B4-17

Correlation between viral production and carbon mineralization under nitrate-reducing conditions in aquifer sediment
journal, March 2014


Effects of suspended matter quality and virus abundance on microbial parameters: experimental evidence from a large European river
journal, October 2009

  • Kernegger, L.; Zweimüller, I.; Peduzzi, P.
  • Aquatic Microbial Ecology, Vol. 57
  • DOI: 10.3354/ame01341

Prokaryotes: The unseen majority
journal, June 1998

  • Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
  • DOI: 10.1073/pnas.95.12.6578

Stimulating the In Situ Activity of Geobacter Species To Remove Uranium from the Groundwater of a Uranium-Contaminated Aquifer
journal, October 2003


Macro- and Micromorphology of Subsurface Carbon in Riparian Zone Soils
journal, January 2005

  • Blazejewski, Gary A.; Stolt, Mark H.; Gold, Arthur J.
  • Soil Science Society of America Journal, Vol. 69, Issue 4
  • DOI: 10.2136/sssaj2004.0145

Viral abundance in aquatic systems:a comparison between marine and fresh waters
journal, January 1995


Virioplankton Abundance in Trophic Gradients of an Upwelling Field
journal, January 2009


Bacterial and Virus-Like Particle Abundances in Purged and Unpurged Groundwater Depth Profiles
journal, March 2012


Distribution of viruses and bacteria in relation to diagenetic activity in an estuarine sediment
journal, July 2003

  • Middelboe, Mathias; Glud, Ronnie N.; Finster, Kai
  • Limnology and Oceanography, Vol. 48, Issue 4
  • DOI: 10.4319/lo.2003.48.4.1447

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Physico-Chemical Heterogeneity of Organic-Rich Sediments in the Rifle Aquifer, CO: Impact on Uranium Biogeochemistry
journal, December 2015

  • Janot, Noémie; Lezama Pacheco, Juan S.; Pham, Don Q.
  • Environmental Science & Technology, Vol. 50, Issue 1
  • DOI: 10.1021/acs.est.5b03208

Soil burial contributes to deep soil organic carbon storage
journal, February 2014


Metabolic and structural response of hyporheic microbial communities to variations in supply of dissolved organic matter
journal, July 2003

  • Findlay, Stuart E. G.; Sinsabaugh, Robert L.; Sobczak, William V.
  • Limnology and Oceanography, Vol. 48, Issue 4
  • DOI: 10.4319/lo.2003.48.4.1608

Dissolved Organic Carbon Influences Microbial Community Composition and Diversity in Managed Aquifer Recharge Systems
journal, July 2012

  • Li, Dong; Sharp, Jonathan O.; Saikaly, Pascal E.
  • Applied and Environmental Microbiology, Vol. 78, Issue 19
  • DOI: 10.1128/AEM.01223-12

Thermodynamically controlled preservation of organic carbon in floodplains
journal, May 2017

  • Boye, Kristin; Noël, Vincent; Tfaily, Malak M.
  • Nature Geoscience, Vol. 10, Issue 6
  • DOI: 10.1038/ngeo2940

Counting Viruses and Bacteria in Photosynthetic Microbial Mats
journal, January 2015

  • Carreira, Cátia; Staal, Marc; Middelboe, Mathias
  • Applied and Environmental Microbiology, Vol. 81, Issue 6
  • DOI: 10.1128/AEM.02863-14

Marine viruses — major players in the global ecosystem
journal, October 2007


Virioplankton: Viruses in Aquatic Ecosystems
journal, March 2000


The Deep Viriosphere: Assessing the Viral Impact on Microbial Community Dynamics in the Deep Subsurface
journal, January 2013

  • Anderson, R. E.; Brazelton, W. J.; Baross, J. A.
  • Reviews in Mineralogy and Geochemistry, Vol. 75, Issue 1
  • DOI: 10.2138/rmg.2013.75.20

Elemental Composition (C, N, P) and Cell Volume of Exponentially Growing and Nutrient-Limited Bacterioplankton
journal, June 2002


Oxygenation of anoxic water in a fluctuating water table system: an experimental and numerical study
journal, April 2000


Geochemical, mineralogical and microbiological characteristics of sediment from a naturally reduced zone in a uranium-contaminated aquifer
journal, August 2012


Short-term variations of virus-like particles in a tropical lake: Relationship with microbial communities (bacteria, ciliates and flagellates)
journal, January 2009

  • Araújo, Magnólia Fernandes Florêncio de; Godinho, Mirna J. L.
  • Microbiological Research, Vol. 164, Issue 4
  • DOI: 10.1016/j.micres.2007.02.011

Subsurface viruses and bacteria in Holocene/Late Pleistocene sediments of Saanich Inlet, BC: ODP Holes 1033B and 1034B, Leg 169S
journal, March 2001


Environmental influences on virus-host interactions in an Australian subtropical reservoir: Virus-host interactions in the sub-tropics
journal, November 2011


Adenosine 3':5'-Cyclic Monophosphate Concentration in the Bacterial Host Regulates the Viral Decision between Lysogeny and Lysis
journal, September 1971

  • Hong, J. -S.; Smith, G. R.; Ames, B. N.
  • Proceedings of the National Academy of Sciences, Vol. 68, Issue 9
  • DOI: 10.1073/pnas.68.9.2258

Seasonal patterns of viruses, bacteria and dissolved organic carbon in a riverine wetland
journal, May 2003


Viruses in granitic groundwater from 69 to 450 m depth of the Äspö hard rock laboratory, Sweden
journal, February 2008

  • Kyle, Jennifer E.; Eydal, Hallgerd S. C.; Ferris, F. Grant
  • The ISME Journal, Vol. 2, Issue 5
  • DOI: 10.1038/ismej.2008.18

Large-Scale Spatial Distribution of Virioplankton in the Adriatic Sea: Testing the Trophic State Control Hypothesis
journal, May 2003


Viruses in the plankton of freshwater and saline Antarctic lakes
journal, September 2001


Virus removal and inactivation by iron (hydr)oxide-mediated Fenton-like processes under sunlight and in the dark
journal, January 2013

  • Nieto-Juarez, Jessica I.; Kohn, Tamar
  • Photochemical & Photobiological Sciences, Vol. 12, Issue 9
  • DOI: 10.1039/c3pp25314g

Biogeochemical Hot Spots and Hot Moments at the Interface of Terrestrial and Aquatic Ecosystems
journal, June 2003


Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla
journal, October 2013


Bacteriophage T4 Development Depends on the Physiology of its Host Escherichia Coli
journal, January 1997


Global distribution of microbial abundance and biomass in subseafloor sediment
journal, August 2012

  • Kallmeyer, J.; Pockalny, R.; Adhikari, R. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 40
  • DOI: 10.1073/pnas.1203849109

Distribution of virus-like Particles in an Oligotrophic Marine Environment (Alboran Sea, Western Mediterranean)
journal, October 2001


Effects of virus infection on respiration rates of marine phytoplankton and microplankton communities
journal, January 2003

  • Eissler, Y.; Sahlsten, E.; Quiñones, Ra
  • Marine Ecology Progress Series, Vol. 262
  • DOI: 10.3354/meps262071

Regulation of bacterial metabolic activity by dissolved organic carbon and viruses: INTERACTION OF VIRUSES-BACTERIA-DOC
journal, November 2013

  • Xu, Jie; Jing, Hongmei; Sun, Mingming
  • Journal of Geophysical Research: Biogeosciences, Vol. 118, Issue 4
  • DOI: 10.1002/2013jg002296

Lytic to temperate switching of viral communities
journal, March 2016

  • Knowles, B.; Silveira, C. B.; Bailey, B. A.
  • Nature, Vol. 531, Issue 7595
  • DOI: 10.1038/nature17193

Variation in Bioavailability of Dissolved Organic Carbon Among Stream Hyporheic Flowpaths
journal, November 2002


Microbial Incorporation of 13 C-Labeled Acetate at the Field Scale:  Detection of Microbes Responsible for Reduction of U(VI)
journal, December 2005

  • Chang, Yun-Juan; Long, Philip E.; Geyer, Roland
  • Environmental Science & Technology, Vol. 39, Issue 23
  • DOI: 10.1021/es051218u

Virus Production and Lysate Recycling in Different Sub-basins of the Northern Baltic Sea
journal, April 2010


Microbiological and Geochemical Heterogeneity in an In Situ Uranium Bioremediation Field Site
journal, October 2005


Interpolation techniques and associated software for environmental data
journal, May 2010

  • Akkala, Arjun; Devabhaktuni, Vijay; Kumar, Ashok
  • Environmental Progress & Sustainable Energy, Vol. 29, Issue 2
  • DOI: 10.1002/ep.10455

Viral Density and Virus-to-Bacterium Ratio in Deep-Sea Sediments of the Eastern Mediterranean
journal, May 2000


Regeneration of dissolved organic matter by viral lysis in marine microbial communities
journal, January 2002


Microscale patchiness of virioplankton
journal, April 2006

  • Seymour, J. R.; Seuront, L.; Doubell, M.
  • Journal of the Marine Biological Association of the United Kingdom, Vol. 86, Issue 3
  • DOI: 10.1017/S0025315406013464

Evidence of Geobacter-associated phage in a uranium-contaminated aquifer
journal, August 2014

  • Holmes, Dawn E.; Giloteaux, Ludovic; Chaurasia, Akhilesh K.
  • The ISME Journal, Vol. 9, Issue 2
  • DOI: 10.1038/ismej.2014.128

Acetate Availability and its Influence on Sustainable Bioremediation of Uranium-Contaminated Groundwater
journal, June 2011


Denitrification in riparian buffer zones: the role of floodplain hydrology
journal, July 1999


Virus-Bacterium Interactions in Water and Sediment of West African Inland Aquatic Systems
journal, August 2006

  • Bettarel, Y.; Bouvy, M.; Dumont, C.
  • Applied and Environmental Microbiology, Vol. 72, Issue 8
  • DOI: 10.1128/AEM.00863-06

Viruses in the sea
journal, September 2005


Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer
journal, March 2014

  • Wrighton, Kelly C.; Castelle, Cindy J.; Wilkins, Michael J.
  • The ISME Journal, Vol. 8, Issue 7
  • DOI: 10.1038/ismej.2013.249

Uranium in Framboidal Pyrite from a Naturally Bioreduced Alluvial Sediment
journal, November 2009

  • Qafoku, Nikolla P.; Kukkadapu, Ravi K.; McKinley, James P.
  • Environmental Science & Technology, Vol. 43, Issue 22
  • DOI: 10.1021/es9017333

Removal and Inactivation of Waterborne Viruses Using Zerovalent Iron
journal, December 2005

  • You, Youwen; Han, Jie; Chiu, Pei C.
  • Environmental Science & Technology, Vol. 39, Issue 23
  • DOI: 10.1021/es050829j

High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments
journal, January 2014

  • Engelhardt, Tim; Kallmeyer, Jens; Cypionka, Heribert
  • The ISME Journal, Vol. 8, Issue 7
  • DOI: 10.1038/ismej.2013.245

Surface Water Linkages Regulate Trophic Interactions in a Groundwater Food Web
journal, September 2011


Persistence of uranium groundwater plumes: Contrasting mechanisms at two DOE sites in the groundwater–river interaction zone
journal, April 2013


Virio- and Bacterioplankton Microscale Distributions at the Sediment-Water Interface
journal, July 2014


Diverse uncultivated ultra-small bacterial cells in groundwater
journal, February 2015

  • Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7372

Soil Organic Carbon Pools in Riparian Landscapes of Southern New England
journal, January 2013

  • Ricker, Matthew C.; Stolt, Mark H.; Donohue, Sean W.
  • Soil Science Society of America Journal, Vol. 77, Issue 3
  • DOI: 10.2136/sssaj2012.0297

Variability of subseafloor viral abundance at the geographically and geologically distinct continental margins
journal, December 2013

  • Yanagawa, Katsunori; Morono, Yuki; Yoshida-Takashima, Yukari
  • FEMS Microbiology Ecology, Vol. 88, Issue 1
  • DOI: 10.1111/1574-6941.12269

Distributions of Virus-Like Particles and Prokaryotes within Microenvironments
journal, January 2016


Impact of hydrology on free-living and particle-associated microorganisms in a river floodplain system (Danube, Austria)
journal, June 2007


Breakdown and microbial uptake of marine viruses and other lysis products
journal, January 1999


Virus-Bacterium Coupling Driven by both Turbidity and Hydrodynamics in an Amazonian Floodplain Lake
journal, September 2010

  • Barros, N.; Farjalla, V. F.; Soares, M. C.
  • Applied and Environmental Microbiology, Vol. 76, Issue 21
  • DOI: 10.1128/AEM.01161-10

Virus dynamics in a large epishelf lake (Beaver Lake, Antarctica)
journal, April 2013

  • Laybourn-Parry, Johanna; Anesio, Alexandre M.; Madan, Nanette
  • Freshwater Biology, Vol. 58, Issue 7
  • DOI: 10.1111/fwb.12146

Natural and anthropogenic forcing on the dynamics of virioplankton in the Yangtze river estuary
journal, April 2006

  • Jiao, Nianzhi; Zhao, Yanlin; Luo, Tingwei
  • Journal of the Marine Biological Association of the United Kingdom, Vol. 86, Issue 3
  • DOI: 10.1017/S0025315406013452

Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I
journal, February 2007

  • Patel, Anand; Noble, Rachel T.; Steele, Joshua A.
  • Nature Protocols, Vol. 2, Issue 2
  • DOI: 10.1038/nprot.2007.6

A colicin-tolerant mutant of Escherichia coli with reduced levels of cyclic AMP and a strong bias towards ? lysogeny
journal, January 1973

  • Rolfe, Barry; Schell, Jozef; Becker, Andrew
  • MGG Molecular & General Genetics, Vol. 120, Issue 1
  • DOI: 10.1007/BF00332980

Macroscale distribution of virioplankton and heterotrophic bacteria in the Bohai Sea
journal, January 2016

  • Wang, Caixia; Wang, Yibo; Paterson, James S.
  • FEMS Microbiology Ecology, Vol. 92, Issue 3
  • DOI: 10.1093/femsec/fiw017

Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016

  • Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13219

Marine viruses and their biogeochemical and ecological effects
journal, June 1999

  • Fuhrman, Jed A.
  • Nature, Vol. 399, Issue 6736
  • DOI: 10.1038/21119

Horizontal and Vertical Distribution of Marine Virioplankton: A Basin Scale Investigation Based on a Global Cruise
journal, November 2014


Organic Carbon Supply and Metabolism in a Shallow Groundwater Ecosystem
journal, November 2000


Re-examination of the relationship between marine virus and microbial cell abundances
journal, January 2016

  • Wigington, Charles H.; Sonderegger, Derek; Brussaard, Corina P. D.
  • Nature Microbiology, Vol. 1, Issue 3
  • DOI: 10.1038/nmicrobiol.2015.24

Spatial Distribution of Carbon in the Subsurface of Riparian Zones
journal, January 2009

  • Blazejewski, Gary A.; Stolt, Mark H.; Gold, Arthur J.
  • Soil Science Society of America Journal, Vol. 73, Issue 5
  • DOI: 10.2136/sssaj2007.0386

Natural Uranium Contamination in Major U.S. Aquifers Linked to Nitrate
journal, July 2015


Geochemical and mineralogical investigation of uranium in multi-element contaminated, organic-rich subsurface sediment
journal, March 2014


Intensified organic carbon dynamics in the ground water of a restored riparian zone: Organic carbon in riparian aquifers
journal, June 2012


Dynamic of Virioplankton Abundance and Its Environmental Control in the Charente Estuary (France)
journal, October 2005


    Works referencing / citing this record:

    Microbial Communities of Low Temperature, Saline Groundwater Used for Therapeutical Purposes in North Poland
    journal, January 2019