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Title: Multiscale Investigation on Biofilm Distribution and Its Impact on Macroscopic Biogeochemical Reaction Rates

Abstract

Biofilms are critical locations for biogeochemical reactions in the subsurface environment. The occurrence and distribution of biofilms at microscale as well as their impacts on macroscopic biogeochemical reaction rates are still poorly understood. This paper investigated the formation and distributions of biofilms in heterogeneous sediments using multiscale models, and evaluated the effects of biofilm heterogeneity on local and macroscopic biogeochemical reaction rates. Sediment pore structures derived from X-ray computed tomography were used to simulate the microscale flow dynamics and biofilm distribution in the sediment column. The response of biofilm formation and distribution to the variations in hydraulic and chemical properties was first examined. One representative biofilm distribution was then utilized to evaluate its effects on macroscopic reaction rates using nitrate reduction as an example. The results revealed that microorganisms primarily grew on the surfaces of grains and aggregates near preferential flow paths where both electron donor and acceptor were readily accessible, leading to the heterogeneous distribution of biofilms in the sediments. Furthermore, the heterogeneous biofilm distribution decreased the macroscopic rate of biogeochemical reactions as compared with those in homogeneous cases. Operationally considering the heterogeneous biofilm distribution in macroscopic reactive transport models such as using dual porosity domain concept can significantlymore » improve the prediction of biogeochemical reaction rates. Overall, this study provided important insights into the biofilm formation and distribution in soils and sediments as well as their impacts on the macroscopic manifestation of reaction rates.« less

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]
  1. Tianjin Univ., (China); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Southern Univ. of Science and Technology, Shenzhen (China)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Nanjing Univ. (China)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Natural Science Foundation of China; Southern University of Science and Technology; Ministry of Science and Technology of China; National Key R&D Program China
OSTI Identifier:
1430450
Alternate Identifier(s):
OSTI ID: 1407819
Report Number(s):
PNNL-SA-123939
Journal ID: ISSN 0043-1397; 49369; KP1702010
Grant/Contract Number:  
AC05-76RL01830; G01296001; 2016YFA0601000; 2016YF0601002
Resource Type:
Accepted Manuscript
Journal Name:
Water Resources Research
Additional Journal Information:
Journal Volume: 53; Journal Issue: 11; Journal ID: ISSN 0043-1397
Publisher:
American Geophysical Union (AGU)
Country of Publication:
United States
Language:
English
Subject:
42 ENGINEERING; Environmental Molecular Sciences Laboratory; multiscale; biofilm; heterogeneity; biogeochemical reaction; scaling

Citation Formats

Yan, Zhifeng, Liu, Chongxuan, Liu, Yuanyuan, and Bailey, Vanessa L. Multiscale Investigation on Biofilm Distribution and Its Impact on Macroscopic Biogeochemical Reaction Rates. United States: N. p., 2017. Web. doi:10.1002/2017WR020570.
Yan, Zhifeng, Liu, Chongxuan, Liu, Yuanyuan, & Bailey, Vanessa L. Multiscale Investigation on Biofilm Distribution and Its Impact on Macroscopic Biogeochemical Reaction Rates. United States. doi:10.1002/2017WR020570.
Yan, Zhifeng, Liu, Chongxuan, Liu, Yuanyuan, and Bailey, Vanessa L. Mon . "Multiscale Investigation on Biofilm Distribution and Its Impact on Macroscopic Biogeochemical Reaction Rates". United States. doi:10.1002/2017WR020570. https://www.osti.gov/servlets/purl/1430450.
@article{osti_1430450,
title = {Multiscale Investigation on Biofilm Distribution and Its Impact on Macroscopic Biogeochemical Reaction Rates},
author = {Yan, Zhifeng and Liu, Chongxuan and Liu, Yuanyuan and Bailey, Vanessa L.},
abstractNote = {Biofilms are critical locations for biogeochemical reactions in the subsurface environment. The occurrence and distribution of biofilms at microscale as well as their impacts on macroscopic biogeochemical reaction rates are still poorly understood. This paper investigated the formation and distributions of biofilms in heterogeneous sediments using multiscale models, and evaluated the effects of biofilm heterogeneity on local and macroscopic biogeochemical reaction rates. Sediment pore structures derived from X-ray computed tomography were used to simulate the microscale flow dynamics and biofilm distribution in the sediment column. The response of biofilm formation and distribution to the variations in hydraulic and chemical properties was first examined. One representative biofilm distribution was then utilized to evaluate its effects on macroscopic reaction rates using nitrate reduction as an example. The results revealed that microorganisms primarily grew on the surfaces of grains and aggregates near preferential flow paths where both electron donor and acceptor were readily accessible, leading to the heterogeneous distribution of biofilms in the sediments. Furthermore, the heterogeneous biofilm distribution decreased the macroscopic rate of biogeochemical reactions as compared with those in homogeneous cases. Operationally considering the heterogeneous biofilm distribution in macroscopic reactive transport models such as using dual porosity domain concept can significantly improve the prediction of biogeochemical reaction rates. Overall, this study provided important insights into the biofilm formation and distribution in soils and sediments as well as their impacts on the macroscopic manifestation of reaction rates.},
doi = {10.1002/2017WR020570},
journal = {Water Resources Research},
number = 11,
volume = 53,
place = {United States},
year = {2017},
month = {9}
}

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Works referenced in this record:

The Electrical Resistivity Log as an Aid in Determining Some Reservoir Characteristics
journal, December 1942

  • Archie, G. E.
  • Transactions of the AIME, Vol. 146, Issue 01
  • DOI: 10.2118/942054-G

Nonpoint Pollution of Surface Waters with Phosphorus and Nitrogen
journal, August 1998


A new combined differential-discrete cellular automaton approach for biofilm modeling: Application for growth in gel beads
journal, March 1998


Intercomparison of 3D pore-scale flow and solute transport simulation methods
journal, September 2016


Pore-Scale Model for Reactive Transport and Biomass Growth
journal, January 2009

  • Tartakovsky, Alexandre M.; Scheibe, Timothy D.; Meakin, Paul
  • Journal of Porous Media, Vol. 12, Issue 5
  • DOI: 10.1615/JPorMedia.v12.i5.30

Biofilm growth in porous media: Experiments, computational modeling at the porescale, and upscaling
journal, September 2016


Localization of soil organic matter in soil aggregates using synchrotron-based X-ray microtomography
journal, November 2014


A hybrid pore-scale and continuum-scale model for solute diffusion, reaction, and biofilm development in porous media
journal, March 2015

  • Tang, Youneng; Valocchi, Albert J.; Werth, Charles J.
  • Water Resources Research, Vol. 51, Issue 3
  • DOI: 10.1002/2014WR016322

Influence of hydrodynamics and nutrients on biofilm structure
journal, December 1998


Soil carbon and nitrogen mineralization: Theory and models across scales
journal, July 2009


Pore-scale and multiscale numerical simulation of flow and transport in a laboratory-scale column
journal, February 2015

  • Scheibe, Timothy D.; Perkins, William A.; Richmond, Marshall C.
  • Water Resources Research, Vol. 51, Issue 2
  • DOI: 10.1002/2014WR015959

Connecting bacterial colonization to physical and biochemical changes in a sand box infiltration experiment
journal, September 2014


Macropores and water flow in soils revisited: REVIEW
journal, June 2013

  • Beven, Keith; Germann, Peter
  • Water Resources Research, Vol. 49, Issue 6
  • DOI: 10.1002/wrcr.20156

Microbial Degradation of Perchlorate: Principles and Applications
journal, September 2003


Average momentum equation for interdendritic flow in a solidifying columnar mushy zone
journal, August 2002

  • Bousquet-Melou, P.; Goyeau, B.; Quintard, M.
  • International Journal of Heat and Mass Transfer, Vol. 45, Issue 17
  • DOI: 10.1016/S0017-9310(02)00077-7

The sensitivity of soil respiration to soil temperature, moisture, and carbon supply at the global scale
journal, October 2016

  • Hursh, Andrew; Ballantyne, Ashley; Cooper, Leila
  • Global Change Biology, Vol. 23, Issue 5
  • DOI: 10.1111/gcb.13489

Two-relaxation-time lattice Boltzmann method and its application to advective-diffusive-reactive transport
journal, November 2017


Biofilm Formation as Microbial Development
journal, October 2000

  • O'Toole, George; Kaplan, Heidi B.; Kolter, Roberto
  • Annual Review of Microbiology, Vol. 54, Issue 1, p. 49-79
  • DOI: 10.1146/annurev.micro.54.1.49

Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review
journal, June 2007


Distribution of Microbial Biomass and Potential for Anaerobic Respiration in Hanford Site 300 Area Subsurface Sediment
journal, December 2011

  • Lin, Xueju; Kennedy, David; Peacock, Aaron
  • Applied and Environmental Microbiology, Vol. 78, Issue 3
  • DOI: 10.1128/AEM.07404-11

99 Tc(VII) Retardation, Reduction, and Redox Rate Scaling in Naturally Reduced Sediments
journal, November 2015

  • Liu, Yuanyuan; Liu, Chongxuan; Kukkadapu, Ravi K.
  • Environmental Science & Technology, Vol. 49, Issue 22
  • DOI: 10.1021/acs.est.5b03273

Coupled transport and reaction kinetics control the nitrate source-sink function of hyporheic zones: HYPORHEIC N SOURCE-SINK CONTROLS
journal, November 2012

  • Zarnetske, Jay P.; Haggerty, Roy; Wondzell, Steven M.
  • Water Resources Research, Vol. 48, Issue 11
  • DOI: 10.1029/2012WR011894

Scale-dependent desorption of uranium from contaminated subsurface sediments: SCALE-DEPENDENT DESORPTION OF URANIUM
journal, August 2008

  • Liu, Chongxuan; Zachara, John M.; Qafoku, Nikolla P.
  • Water Resources Research, Vol. 44, Issue 8
  • DOI: 10.1029/2007WR006478

Biofilms: Microbial Life on Surfaces
journal, September 2002


Uranium Bioreduction Rates across Scales: Biogeochemical Hot Moments and Hot Spots during a Biostimulation Experiment at Rifle, Colorado
journal, August 2014

  • Bao, Chen; Wu, Hongfei; Li, Li
  • Environmental Science & Technology, Vol. 48, Issue 17
  • DOI: 10.1021/es501060d

Saturated Hydraulic Conductivity Reduction Caused by Aerobic Bacteria in Sand Columns
journal, January 1992


Modeling soil moisture and oxygen effects on soil biogeochemical cycles including dissimilatory nitrate reduction to ammonium (DNRA)
journal, December 2013


Microbial hotspots and hot moments in soil: Concept & review
journal, April 2015


Environmental Impact and Mechanisms of the Biological Clogging of Saturated Soils and Aquifer Materials
journal, April 1998

  • Baveye, Philippe; Vandevivere, Philippe; Hoyle, Blythe L.
  • Critical Reviews in Environmental Science and Technology, Vol. 28, Issue 2
  • DOI: 10.1080/10643389891254197

Extracellular Polymeric Substances Affecting Pore-Scale Hydrologic Conditions for Bacterial Activity in Unsaturated Soils
journal, January 2007

  • Or, Dani; Phutane, Sachin; Dechesne, Arnaud
  • Vadose Zone Journal, Vol. 6, Issue 2
  • DOI: 10.2136/vzj2006.0080

A mechanistic model (BCC-PSSICO) to predict changes in the hydraulic properties for bio-amended variably saturated soils: BCC-PSSICO MODEL
journal, January 2017

  • Carles Brangarí, Albert; Sanchez-Vila, Xavier; Freixa, Anna
  • Water Resources Research, Vol. 53, Issue 1
  • DOI: 10.1002/2015WR018517

Biogeochemical Processes and Microbial Characteristics across Groundwater−Surface Water Boundaries of the Hanford Reach of the Columbia River
journal, November 2003

  • Moser, Duane P.; Fredrickson, James K.; Geist, David R.
  • Environmental Science & Technology, Vol. 37, Issue 22
  • DOI: 10.1021/es034457v

Biological clogging of sand and changes of organic constituents during artificial recharge
journal, January 1983


Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways
journal, March 2007


Biofilm development and the dynamics of preferential flow paths in porous media
journal, October 2013


Denitrification potential in subsoils: A mechanism to reduce nitrate leaching to groundwater
journal, January 2012


Coupled Hydro-Biogeochemical Processes Controlling Cr Reductive Immobilization in Columbia River Hyporheic Zone
journal, January 2017

  • Liu, Yuanyuan; Xu, Fen; Liu, Chongxuan
  • Environmental Science & Technology, Vol. 51, Issue 3
  • DOI: 10.1021/acs.est.6b05099

Effect of shear stress and growth conditions on detachment and physical properties of biofilms
journal, November 2012


Artificial groundwater treatment: biofilm activity and organic carbon removal performance
journal, February 2004


Microbial Biofilms: from Ecology to Molecular Genetics
journal, December 2000


The effect of biofilm permeability on bio-clogging of porous media
journal, December 2011

  • Pintelon, Thomas R. R.; Picioreanu, Cristian; van Loosdrecht, Mark C. M.
  • Biotechnology and Bioengineering, Vol. 109, Issue 4
  • DOI: 10.1002/bit.24381

Geochemical and transport properties of dissolved organic carbon in a clay-rich aquitard: DOC IN AQUITARDS
journal, July 2003

  • Hendry, M. Jim; Ranville, J. R.; Boldt-Leppin, B. E. J.
  • Water Resources Research, Vol. 39, Issue 7
  • DOI: 10.1029/2002WR001943

Preferential flow paths: biological ‘hot spots’ in soils
journal, May 2001


Computational pore network modeling of the influence of biofilm permeability on bioclogging in porous media
journal, January 2008

  • Thullner, Martin; Baveye, Philippe
  • Biotechnology and Bioengineering, Vol. 99, Issue 6
  • DOI: 10.1002/bit.21708

An improved pore-scale biofilm model and comparison with a microfluidic flow cell experiment: A PORE-SCALE BIOFILM MODEL AND COMPARISON WITH AN EXPERIMENT
journal, December 2013

  • Tang, Youneng; Valocchi, Albert J.; Werth, Charles J.
  • Water Resources Research, Vol. 49, Issue 12
  • DOI: 10.1002/2013WR013843

Pore-scale imaging and modelling
journal, January 2013


Nitrate reduction in streambed sediments: Effects of flow and biogeochemical kinetics: NITRATE ATTENUATION DURING GROUNDWATER DISCHARGE
journal, December 2007

  • Gu, Chuanhui; Hornberger, George M.; Mills, Aaron L.
  • Water Resources Research, Vol. 43, Issue 12
  • DOI: 10.1029/2007WR006027

Comparison of bioclogging effects in saturated porous media within one- and two-dimensional flow systems
journal, February 2010


Pore-Scale Process Coupling and Effective Surface Reaction Rates in Heterogeneous Subsurface Materials
journal, January 2015

  • Liu, Chongxuan; Liu, Yuanyuan; Kerisit, Sebastien
  • Reviews in Mineralogy and Geochemistry, Vol. 80, Issue 1
  • DOI: 10.2138/rmg.2015.80.06

Soil Matrix and Macropore Biodegradation of 2,4-D
journal, January 1995


Hyporheic flow and transport processes: Mechanisms, models, and biogeochemical implications: HYPORHEIC FLOW AND TRANSPORT PROCESSES
journal, October 2014

  • Boano, F.; Harvey, J. W.; Marion, A.
  • Reviews of Geophysics, Vol. 52, Issue 4
  • DOI: 10.1002/2012RG000417

The Impact of Sub-Resolution Porosity of X-ray Microtomography Images on the Permeability
journal, April 2016

  • Soulaine, Cyprien; Gjetvaj, Filip; Garing, Charlotte
  • Transport in Porous Media, Vol. 113, Issue 1
  • DOI: 10.1007/s11242-016-0690-2

Vadose zone oxygen (O2) dynamics during drying and wetting cycles: An artificial recharge laboratory experiment
journal, August 2015


Scale-dependent rates of uranyl surface complexation reaction in sediments
journal, March 2013

  • Liu, Chongxuan; Shang, Jianying; Kerisit, Sebastien
  • Geochimica et Cosmochimica Acta, Vol. 105
  • DOI: 10.1016/j.gca.2012.12.003

Soil O 2 controls denitrification rates and N 2 O yield in a riparian wetland : SOIL O
journal, February 2012

  • Burgin, Amy J.; Groffman, Peter M.
  • Journal of Geophysical Research: Biogeosciences, Vol. 117, Issue G1
  • DOI: 10.1029/2011JG001799

Pore and continuum scale study of the effect of subgrid transport heterogeneity on redox reaction rates
journal, August 2015


A dual-domain mass transfer approach for modeling solute transport in heterogeneous aquifers: Application to the Macrodispersion Experiment (MADE) site
journal, September 2000

  • Feehley, C. Erin; Zheng, Chunmiao; Molz, Fred J.
  • Water Resources Research, Vol. 36, Issue 9
  • DOI: 10.1029/2000WR900148

Microbial activity in response to water-filled pore space of variably eroded southern Piedmont soils
journal, January 1999


Mechanisms of Dissolved Organic Carbon Adsorption on Soil
journal, January 1989


Impact of flow velocity on biochemical processes – a laboratory experiment
journal, January 2014

  • Boisson, A.; Roubinet, D.; Aquilina, L.
  • Hydrology and Earth System Sciences Discussions, Vol. 11, Issue 8
  • DOI: 10.5194/hessd-11-9829-2014

The ecology and biogeochemistry of stream biofilms
journal, March 2016

  • Battin, Tom J.; Besemer, Katharina; Bengtsson, Mia M.
  • Nature Reviews Microbiology, Vol. 14, Issue 4
  • DOI: 10.1038/nrmicro.2016.15

Denitrification Across Landscapes and Waterscapes: a Synthesis
journal, December 2006


Density, porosity, and pore structure of biofilms
journal, November 1994


2D visualization captures the local heterogeneity of oxidative metabolism across soils from diverse land-use
journal, December 2016


Spatial location of carbon decomposition in the soil pore system
journal, December 2004


Organic matter stabilization in soil microaggregates: implications from spatial heterogeneity of organic carbon contents and carbon forms
journal, March 2007


Micro-continuum Approach for Pore-Scale Simulation of Subsurface Processes
journal, May 2016


The effects of sediment depth and oxygen concentration on the use of organic matter: An experimental study using an infiltration sediment tank
journal, January 2016


Imaging biofilm architecture within porous media using synchrotron-based X-ray computed microtomography: TECHNICAL NOTE
journal, February 2011

  • Iltis, Gabriel C.; Armstrong, Ryan T.; Jansik, Danielle P.
  • Water Resources Research, Vol. 47, Issue 2
  • DOI: 10.1029/2010WR009410

Groundwater–Surface Water Relationships in Boreal Forest Watersheds: Dissolved Organic Carbon and Inorganic Nutrient Dynamics
journal, January 1989

  • Ford, T. E.; Naiman, Robert J.
  • Canadian Journal of Fisheries and Aquatic Sciences, Vol. 46, Issue 1
  • DOI: 10.1139/f89-006

Macropores and water flow in soils
journal, October 1982


A Unified Multiscale Model for Pore-ScaleFlow Simulations in Soils
journal, January 2014

  • Yang, Xiaofan; Liu, Chongxuan; Shang, Jianying
  • Soil Science Society of America Journal, Vol. 78, Issue 1
  • DOI: 10.2136/sssaj2013.05.0190

Effect of Subgrid Heterogeneity on Scaling Geochemical and Biogeochemical Reactions: A Case of U(VI) Desorption
journal, January 2014

  • Liu, Chongxuan; Shang, Jianying; Shan, Huimei
  • Environmental Science & Technology, Vol. 48, Issue 3
  • DOI: 10.1021/es404224j

Contributions of microbial biofilms to ecosystem processes in stream mesocosms
journal, November 2003

  • Battin, Tom J.; Kaplan, Louis A.; Denis Newbold, J.
  • Nature, Vol. 426, Issue 6965
  • DOI: 10.1038/nature02152

Pore-scale simulation of biomass growth along the transverse mixing zone of a model two-dimensional porous medium: PORE-SCALE SIMULATION OF BIOMASS GROWTH
journal, July 2005

  • Knutson, C. E.; Werth, C. J.; Valocchi, A. J.
  • Water Resources Research, Vol. 41, Issue 7
  • DOI: 10.1029/2004WR003459

Pore-scale investigation on the response of heterotrophic respiration to moisture conditions in heterogeneous soils
journal, November 2016