Increasing aggregate size reduces single-cell organic carbon incorporation by hydrogel-embedded wetland microbes

Johnston, Juliet T.; Quoc, Bao Nguyen; Abrahamson, Britt; Candry, Pieter; Ramon, Christina; Cash, Kevin J.; Saccomano, Sam C.; Samo, Ty J.; Ye, Congwang; Weber, Peter K.; Winkler, Mari-Karoliina Henriikka; Mayali, Xavier

doi:10.1093/ismeco/ycae086

Title: Increasing aggregate size reduces single-cell organic carbon incorporation by hydrogel-embedded wetland microbes

Journal Article · 20 June 2024 · ISME Communications

DOI: https://doi.org/10.1093/ismeco/ycae086 · OSTI ID:2396057

Johnston, Juliet T.; Quoc, Bao Nguyen; Abrahamson, Britt; Candry, Pieter; Ramon, Christina; Cash, Kevin J.; Saccomano, Sam C.; Samo, Ty J.; Ye, Congwang; Weber, Peter K.; Winkler, Mari-Karoliina Henriikka; Mayali, Xavier

Abstract Microbial degradation of organic carbon in sediments is impacted by the availability of oxygen and substrates for growth. To better understand how particle size and redox zonation impact microbial organic carbon incorporation, techniques that maintain spatial information are necessary to quantify elemental cycling at the microscale. In this study, we produced hydrogel microspheres of various diameters (100, 250, and 500 μm) and inoculated them with an aerobic heterotrophic bacterium isolated from a freshwater wetland (Flavobacterium sp.), and in a second experiment with a microbial community from an urban lacustrine wetland. The hydrogel-embedded microbial populations were incubated with 13C-labeled substrates to quantify organic carbon incorporation into biomass via nanoSIMS. Additionally, luminescent nanosensors enabled spatially explicit measurements of oxygen concentrations inside the microspheres. The experimental data were then incorporated into a reactive-transport model to project long-term steady-state conditions. Smaller (100 μm) particles exhibited the highest microbial cell-specific growth per volume, but also showed higher absolute activity near the surface compared to the larger particles (250 and 500 μm). The experimental results and computational models demonstrate that organic carbon availability was not high enough to allow steep oxygen gradients and as a result, all particle sizes remained well-oxygenated. Our study provides a foundational framework for future studies investigating spatially dependent microbial activity in aggregates using isotopically labeled substrates to quantify growth.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 2396057

Journal Information:: ISME Communications, Journal Name: ISME Communications Journal Issue: 1 Vol. 4; ISSN 2730-6151

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

A new combined differential-discrete cellular automaton approach for biofilm modeling: Application for growth in gel beads Picioreanu, Cristian; van Loosdrecht, Mark C. M.; Heijnen, Joseph J. Biotechnology and Bioengineering, Vol. 57, Issue 6 https://doi.org/10.1002/(SICI)1097-0290(19980320)57:6<718::AID-BIT9>3.0.CO;2-O	journal	March 1998
Hydration and diffusion processes shape microbial community organization and function in model soil aggregates: HYDRATION AFFECTS MICROBIAL ACTIVITY IN SOIL AGGREGATES Ebrahimi, Ali; Or, Dani Water Resources Research, Vol. 51, Issue 12 https://doi.org/10.1002/2015WR017565	journal	December 2015
Structured Macroporous Hydrogels: Progress, Challenges, and Opportunities De France, Kevin J.; Xu, Fei; Hoare, Todd Advanced Healthcare Materials, Vol. 7, Issue 1 https://doi.org/10.1002/adhm.201700927	journal	December 2017
Detecting oxygen consumption in the proximity of Saccharomyces cerevisiae cells using self‐assembled fluorescent nanosensors Kuang, Yina; Walt, David R. Biotechnology and Bioengineering, Vol. 96, Issue 2 https://doi.org/10.1002/bit.21092	journal	July 2006
Modelling microbial competition in nitrifying biofilm reactors Vannecke, T. P. W.; Volcke, E. I. P. Biotechnology and Bioengineering, Vol. 112, Issue 12 https://doi.org/10.1002/bit.25680	journal	August 2015
Hard and soft plastic resin embedding for single-cell element uptake investigations of marine-snow-associated microorganisms using nano-scale secondary ion mass spectrometry: NanoSIMS of sectioned marine snow samples Rogge, Andreas; Flintrop, Clara M.; Iversen, Morten H. Limnology and Oceanography: Methods, Vol. 16, Issue 8 https://doi.org/10.1002/lom3.10261	journal	July 2018
Constructed Wetlands Revisited: Microbial Diversity in the –omics Era Sánchez, Olga Microbial Ecology, Vol. 73, Issue 3 https://doi.org/10.1007/s00248-016-0881-y	journal	November 2016
Organic Carbon Composition and Oxygen Metabolism across a Gradient of Seasonally Inundated Limesink and Riparian Wetlands in the Southeast Coastal Plain, USA Opsahl, Stephen P. Biogeochemistry, Vol. 76, Issue 1 https://doi.org/10.1007/s10533-005-2074-5	journal	October 2005
Influence of Physical Properties of Biomaterials on Cellular Behavior Lin, Susan; Sangaj, Nivedita; Razafiarison, Tojo Pharmaceutical Research, Vol. 28, Issue 6 https://doi.org/10.1007/s11095-011-0378-9	journal	February 2011
Hierarchical encapsulation of bacteria in functional hydrogel beads for inter- and intra- species communication Jeong, Yoon; Irudayaraj, Joseph Acta Biomaterialia, Vol. 158 https://doi.org/10.1016/j.actbio.2023.01.003	journal	March 2023
Tracking microbial interactions with NanoSIMS Musat, Niculina; Musat, Florin; Weber, Peter Kilian Current Opinion in Biotechnology, Vol. 41 https://doi.org/10.1016/j.copbio.2016.06.007	journal	October 2016
Grain size distribution drives microbial communities vertically assemble in nascent lake sediments Lin, Jie; Zhou, Xiaotian; Lu, Xiang Environmental Research, Vol. 227 https://doi.org/10.1016/j.envres.2023.115828	journal	June 2023
Soil pores and their contributions to soil carbon processes Kravchenko, Alexandra N.; Guber, Andrey K. Geoderma, Vol. 287 https://doi.org/10.1016/j.geoderma.2016.06.027	journal	February 2017
Diffusion coefficient of solute in heterogeneous and macroporous hydrogels and its correlation with the effective crosslinking density Tokuyama, Hideaki; Nakahata, Yu; Ban, Takahiko Journal of Membrane Science, Vol. 595 https://doi.org/10.1016/j.memsci.2019.117533	journal	February 2020
Unravelling gradient layers of microbial communities, proteins, and chemical structure in aerobic granules Cydzik-Kwiatkowska, Agnieszka; de Jonge, Nadieh; Poulsen, Jan Struckmann Science of The Total Environment, Vol. 829 https://doi.org/10.1016/j.scitotenv.2022.154253	journal	July 2022
Deciphering the diversity patterns and community assembly of rare and abundant bacterial communities in a wetland system Yang, Yan; Cheng, Kexin; Li, Kaihang Science of The Total Environment, Vol. 838 https://doi.org/10.1016/j.scitotenv.2022.156334	journal	September 2022
Modeling coupled pesticide degradation and organic matter turnover: From gene abundance to process rates Pagel, Holger; Poll, Christian; Ingwersen, Joachim Soil Biology and Biochemistry, Vol. 103 https://doi.org/10.1016/j.soilbio.2016.09.014	journal	December 2016
Multidimensional modelling to investigate interspecies hydrogen transfer in anaerobic biofilms Batstone, D. J.; Picioreanu, C.; van Loosdrecht, M. C. M. Water Research, Vol. 40, Issue 16 https://doi.org/10.1016/j.watres.2006.06.014	journal	September 2006
Modelling simultaneous anaerobic methane and ammonium removal in a granular sludge reactor Winkler, M-K. H.; Ettwig, K. F.; Vannecke, T. P. W. Water Research, Vol. 73 https://doi.org/10.1016/j.watres.2015.01.039	journal	April 2015
Effective nitrogen removal from ammonium-depleted wastewater by partial nitritation and anammox immobilized in granular and thin layer gel carriers Landreau, Matthieu; Byson, Samuel J.; You, HeeJun Water Research, Vol. 183 https://doi.org/10.1016/j.watres.2020.116078	journal	September 2020
Aerobic granular sludge: Impact of size distribution on nitrification capacity Nguyen Quoc, Bao; Wei, Stephany; Armenta, Maxwell Water Research, Vol. 188 https://doi.org/10.1016/j.watres.2020.116445	journal	January 2021
Sustained nitrogen loss in a symbiotic association of Comammox Nitrospira and Anammox bacteria Gottshall, Ekaterina Y.; Bryson, Sam J.; Cogert, Kathryn I. Water Research, Vol. 202 https://doi.org/10.1016/j.watres.2021.117426	journal	September 2021
Unraveling encapsulated growth of Nitrosomonas europaea in alginate: An experimental and modeling study Wang, Zhiyue; Perez-Calleja, Patricia; Nerenberg, Robert Water Research, Vol. 208 https://doi.org/10.1016/j.watres.2021.117857	journal	January 2022
Organic carbon preservation in wetlands: Iron oxide protection vs. thermodynamic limitation Sun, Fu-Sheng; Ma, Chao; Yu, Guang-Hui Water Research, Vol. 241 https://doi.org/10.1016/j.watres.2023.120133	journal	August 2023
Correlated SEM, FIB-SEM, TEM, and NanoSIMS Imaging of Microbes from the Hindgut of a Lower Termite: Methods for In Situ Functional and Ecological Studies of Uncultivable Microbes Carpenter, Kevin J.; Weber, Peter K.; Davisson, M. Lee Microscopy and Microanalysis, Vol. 19, Issue 6 https://doi.org/10.1017/S1431927613013482	journal	October 2013
Simultaneous Determination of Oxygen and pH Inside Microfluidic Devices Using Core–Shell Nanosensors Ehgartner, Josef; Strobl, Martin; Bolivar, Juan M. Analytical Chemistry, Vol. 88, Issue 19 https://doi.org/10.1021/acs.analchem.6b02849	journal	September 2016
Microbe Encapsulation for Selective Rare-Earth Recovery from Electronic Waste Leachates Brewer, Aaron; Dohnalkova, Alice; Shutthanandan, Vaithiyalingam Environmental Science & Technology, Vol. 53, Issue 23 https://doi.org/10.1021/acs.est.9b04608	journal	November 2019
Encapsulation of Autoinducer Sensing Reporter Bacteria in Reinforced Alginate-Based Microbeads Li, Ping; Müller, Mareike; Chang, Matthew Wook ACS Applied Materials & Interfaces, Vol. 9, Issue 27 https://doi.org/10.1021/acsami.7b07166	journal	June 2017
Multi-Scale Individual-Based Model of Microbial and Bioconversion Dynamics in Aerobic Granular Sludge Xavier, Joao B.; de Kreuk, Merle K.; Picioreanu, Cristian Environmental Science & Technology, Vol. 41, Issue 18 https://doi.org/10.1021/es070264m	journal	September 2007
Segregation of Biomass in Cyclic Anaerobic/Aerobic Granular Sludge Allows the Enrichment of Anaerobic Ammonium Oxidizing Bacteria at Low Temperatures Winkler, Mari K. H.; Kleerebezem, Robbert; Kuenen, J. Gijs Environmental Science & Technology, Vol. 45, Issue 17 https://doi.org/10.1021/es201388t	journal	September 2011
NanoSIMS Study of Organic Matter Associated with Soil Aggregates: Advantages, Limitations, and Combination with STXM Remusat, Laurent; Hatton, Pierre-Joseph; Nico, Peter S. Environmental Science & Technology, Vol. 46, Issue 7 https://doi.org/10.1021/es203745k	journal	March 2012
Hydroxylamine Diffusion Can Enhance N ₂ O Emissions in Nitrifying Biofilms: A Modeling Study Sabba, Fabrizio; Picioreanu, Cristian; Pérez, Julio Environmental Science & Technology, Vol. 49, Issue 3 https://doi.org/10.1021/es5046919	journal	January 2015
Ultra-Small, Highly Stable, and Sensitive Dual Nanosensors for Imaging Intracellular Oxygen and pH in Cytosol Wang, Xu-dong; Stolwijk, Judith A.; Lang, Thomas Journal of the American Chemical Society, Vol. 134, Issue 41 https://doi.org/10.1021/ja308830e	journal	October 2012
Microbial diversity along a sediment detrital particle size gradient Yeager, P. E.; Sinsabaugh, R. L. Aquatic Ecology, Vol. 32, Issue 4, p. 281-289 https://doi.org/10.1023/A:1009944328443	journal	December 1998
On Upscaling of Soil Microbial Processes and Biogeochemical Fluxes From Aggregates to Landscapes Ebrahimi, Ali; Or, Dani Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 5 https://doi.org/10.1029/2017JG004347	journal	May 2018
Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides Popa, Radu; Weber, Peter K.; Pett-Ridge, Jennifer The ISME Journal, Vol. 1, Issue 4 https://doi.org/10.1038/ismej.2007.44	journal	July 2007
Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach Woebken, Dagmar; Burow, Luke C.; Behnam, Faris The ISME Journal, Vol. 9, Issue 2 https://doi.org/10.1038/ismej.2014.144	journal	October 2014
Carbon storage in US wetlands Nahlik, A. M.; Fennessy, M. S. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13835	journal	December 2016
Affinity informs environmental cooperation between ammonia-oxidizing archaea (AOA) and anaerobic ammonia-oxidizing (Anammox) bacteria Straka, Levi L.; Meinhardt, Kelley A.; Bollmann, Annette The ISME Journal, Vol. 13, Issue 8 https://doi.org/10.1038/s41396-019-0408-x	journal	April 2019
Active subseafloor microbial communities from Mariana back-arc venting fluids share metabolic strategies across different thermal niches and taxa Trembath-Reichert, Elizabeth; Butterfield, David A.; Huber, Julie A. The ISME Journal, Vol. 13, Issue 9 https://doi.org/10.1038/s41396-019-0431-y	journal	May 2019
Metabolic flexibility allows bacterial habitat generalists to become dominant in a frequently disturbed ecosystem Chen, Ya-Jou; Leung, Pok Man; Wood, Jennifer L. The ISME Journal https://doi.org/10.1038/s41396-021-00988-w	journal	May 2021
Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate Kim, Hyungseok; Kimbrel, Jeffrey A.; Vaiana, Christopher A. The ISME Journal, Vol. 16, Issue 4 https://doi.org/10.1038/s41396-021-01147-x	journal	November 2021
Single-cell isotope tracing reveals functional guilds of bacteria associated with the diatom Phaeodactylum tricornutum Mayali, Xavier; Samo, Ty J.; Kimbrel, Jeff A. Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-41179-9	journal	September 2023
Immobilization of active ammonia-oxidizing archaea in hydrogel beads Landreau, Matthieu; You, HeeJun; Stahl, David A. npj Clean Water, Vol. 4, Issue 1 https://doi.org/10.1038/s41545-021-00134-1	journal	September 2021
Bacteria and archaea on Earth and their abundance in biofilms Flemming, Hans-Curt; Wuertz, Stefan Nature Reviews Microbiology, Vol. 17, Issue 4 https://doi.org/10.1038/s41579-019-0158-9	journal	February 2019
Gradients and consequences of heterogeneity in biofilms Jo, Jeanyoung; Price-Whelan, Alexa; Dietrich, Lars E. P. Nature Reviews Microbiology, Vol. 20, Issue 10 https://doi.org/10.1038/s41579-022-00692-2	journal	February 2022
Hydrogel-based biocontainment of bacteria for continuous sensing and computation Tang, Tzu-Chieh; Tham, Eléonore; Liu, Xinyue Nature Chemical Biology, Vol. 17, Issue 6 https://doi.org/10.1038/s41589-021-00779-6	journal	April 2021
NanoSIMS combined with fluorescence microscopy as a tool for subcellular imaging of isotopically labeled platinum-based anticancer drugs Legin, Anton A.; Schintlmeister, Arno; Jakupec, Michael A. Chemical Science, Vol. 5, Issue 8 https://doi.org/10.1039/C3SC53426J	journal	January 2014
A near-infrared optical nanosensor for measuring aerobic respiration in microbial systems Saccomano, Samuel C.; Cash, Kevin J. The Analyst, Vol. 147, Issue 1 https://doi.org/10.1039/D1AN01855H	journal	January 2022
Effect of heterotrophic growth on autotrophic nitrogen removal in a granular sludge reactor Mozumder, Md. Salatul Islam; Picioreanu, Cristian; van Loosdrecht, Mark C. M. Environmental Technology, Vol. 35, Issue 8 https://doi.org/10.1080/09593330.2013.859711	journal	November 2013
Microorganisms oxidize glucose through distinct pathways in permeable and cohesive sediments Hutchinson, Tess F.; Kessler, Adam J.; Wong, Wei Wen The ISME Journal, Vol. 18, Issue 1 https://doi.org/10.1093/ismejo/wrae001	journal	January 2024
Exploring the oxygen sensitivity of wetland soil carbon mineralization Chapman, Samantha K.; Hayes, Matthew A.; Kelly, Brendan Biology Letters, Vol. 15, Issue 1 https://doi.org/10.1098/rsbl.2018.0407	journal	January 2019
Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles - upscaling an aggregate biophysical model Ebrahimi, Ali; Or, Dani Global Change Biology, Vol. 22, Issue 9 https://doi.org/10.1111/gcb.13345	journal	June 2016
Microbially mediated climate feedbacks from wetland ecosystems Candry, Pieter; Abrahamson, Britt; Stahl, David Allan Global Change Biology, Vol. 29, Issue 18 https://doi.org/10.1111/gcb.16850	journal	June 2023
Spatial location of carbon decomposition in the soil pore system Strong, D. T.; Wever, H. De; Merckx, R. European Journal of Soil Science, Vol. 55, Issue 4 https://doi.org/10.1111/j.1365-2389.2004.00639.x	journal	December 2004
Particle size scales and classification of sediment types based on particle size distributions: Review and recommended procedures Blott, Simon J.; Pye, Kenneth Sedimentology, Vol. 59, Issue 7 https://doi.org/10.1111/j.1365-3091.2012.01335.x	journal	May 2012
A trait-based approach for modelling microbial litter decomposition Allison, S. D. Ecology Letters, Vol. 15, Issue 9 https://doi.org/10.1111/j.1461-0248.2012.01807.x	journal	May 2012
Oxygen and the Spatial Structure of Microbial Communities Fenchel, Tom; Finlay, Bland Biological Reviews, Vol. 83, Issue 4 https://doi.org/10.1111/j.1469-185X.2008.00054.x	journal	October 2008
Stable isotopes and biomarkers in microbial ecology Boschker, H. T. S.; Middelburg, J. J. FEMS Microbiology Ecology, Vol. 40, Issue 2 https://doi.org/10.1111/j.1574-6941.2002.tb00940.x	journal	May 2002
Diffusion in Biofilms Stewart, P. S. Journal of Bacteriology, Vol. 185, Issue 5 https://doi.org/10.1128/JB.185.5.1485-1491.2003	journal	March 2003
A new medium for the enumeration and subculture of bacteria from potable water. Reasoner, D. J.; Geldreich, E. E. Applied and Environmental Microbiology, Vol. 49, Issue 1 https://doi.org/10.1128/aem.49.1.1-7.1985	journal	January 1985
Simulation of multispecies biofilm development in three dimensions Noguera, Daniel R.; Pizarro, Gonzalo; Stahl, David A. Water Science and Technology, Vol. 39, Issue 7 https://doi.org/10.2166/wst.1999.0343	journal	April 1999
Spatial Control of Carbon Dynamics in Soil by Microbial Decomposer Communities Pagel, Holger; Kriesche, Björn; Uksa, Marie Frontiers in Environmental Science, Vol. 8 https://doi.org/10.3389/fenvs.2020.00002	journal	January 2020
Trait-Based Representation of Biological Nitrification: Model Development, Testing, and Predicted Community Composition Bouskill, Nicholas J.; Tang, Jinyun; Riley, William J. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00364	journal	January 2012
Predicting the Responses of Soil Nitrite-Oxidizers to Multi-Factorial Global Change: A Trait-Based Approach Le Roux, Xavier; Bouskill, Nicholas J.; Niboyet, Audrey Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00628	journal	May 2016
Characterizing Chemoautotrophy and Heterotrophy in Marine Archaea and Bacteria With Single-Cell Multi-isotope NanoSIP Dekas, Anne E.; Parada, Alma E.; Mayali, Xavier Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02682	journal	December 2019
A Review of Methods to Determine Viability, Vitality, and Metabolic Rates in Microbiology Braissant, Olivier; Astasov-Frauenhoffer, Monika; Waltimo, Tuomas Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.547458	journal	November 2020

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