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Delineating the Drivers and Functionality of Methanogenic Niches within an Arid Landfill

Microbial communities mediate the transformation of organic matter within landfills into methane (CH(4)). Yet their ecological role in CH(4) production is rarely evaluated. To characterize the microbiome associated with this biotransformation, the overall community and methanogenic Archaea were surv...

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Autores principales: Reynolds, Mark C., Finn, Damien, Sarno, Analissa F., Allen, Richard, Deathrage, J. David, Krajmalnik-Brown, Rosa, Cadillo-Quiroz, Hinsby
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9088289/
https://www.ncbi.nlm.nih.gov/pubmed/35404071
http://dx.doi.org/10.1128/aem.02438-21
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author Reynolds, Mark C.
Finn, Damien
Sarno, Analissa F.
Allen, Richard
Deathrage, J. David
Krajmalnik-Brown, Rosa
Cadillo-Quiroz, Hinsby
author_facet Reynolds, Mark C.
Finn, Damien
Sarno, Analissa F.
Allen, Richard
Deathrage, J. David
Krajmalnik-Brown, Rosa
Cadillo-Quiroz, Hinsby
author_sort Reynolds, Mark C.
collection PubMed
description Microbial communities mediate the transformation of organic matter within landfills into methane (CH(4)). Yet their ecological role in CH(4) production is rarely evaluated. To characterize the microbiome associated with this biotransformation, the overall community and methanogenic Archaea were surveyed in an arid landfill using leachate collected from distinctly aged landfill cells (i.e., younger, intermediate, and older). We hypothesized that distinct methanogenic niches exist within an arid landfill, driven by geochemical gradients that developed under extended and age-dependent waste biodegradation stages. Using 16S rRNA and mcrA gene amplicon sequencing, we identified putative methanogenic niches as follows. The order Methanomicrobiales was the most abundant order in leachate from younger cells, where leachate temperature and propionate concentrations were measured at 41.8°C ± 1.7°C and 57.1 ± 10.7 mg L(−1). In intermediate-aged cells, the family Methanocellaceae was identified as a putative specialist family under intermediate-temperature and -total dissolved solid (TDS) conditions, wherein samples had a higher alpha diversity index and near CH(4) concentrations. In older-aged cells, accumulating metals and TDS supported Methanocorpusculaceae, “Candidatus Bathyarchaeota,” and “Candidatus Verstraetearchaeota” operational taxonomic units (OTUs). Consistent with the mcrA data, we assayed methanogenic activity across the age gradient through stable isotopic measurements of δ(13)C of CH(4) and δ(13)C of CO(2). The majority (80%) of the samples’ carbon fractionation was consistent with hydrogenotrophic methanogenesis. Together, we report age-dependent geochemical gradients detected through leachate in an arid landfill seemingly influencing CH(4) production, niche partitioning, and methanogenic activity. IMPORTANCE Microbiome analysis is becoming common in select municipal and service ecosystems, including wastewater treatment and anaerobic digestion, but its potential as a microbial-status-informative tool to promote or mitigate CH(4) production has not yet been evaluated in landfills. Methanogenesis mediated by Archaea is highly active in solid-waste microbiomes but is commonly neglected in studies employing next-generation sequencing techniques. Identifying methanogenic niches within a landfill offers detail into operations that positively or negatively impact the commercial production of methane known as biomethanation. We provide evidence that the geochemistry of leachate and its microbiome can be a variable accounting for ecosystem-level (coarse) variation of CH(4) production, where we demonstrate through independent assessments of leachate and gas collection that the functional variability of an arid landfill is linked to the composition of methanogenic Archaea.
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spelling pubmed-90882892022-05-11 Delineating the Drivers and Functionality of Methanogenic Niches within an Arid Landfill Reynolds, Mark C. Finn, Damien Sarno, Analissa F. Allen, Richard Deathrage, J. David Krajmalnik-Brown, Rosa Cadillo-Quiroz, Hinsby Appl Environ Microbiol Microbial Ecology Microbial communities mediate the transformation of organic matter within landfills into methane (CH(4)). Yet their ecological role in CH(4) production is rarely evaluated. To characterize the microbiome associated with this biotransformation, the overall community and methanogenic Archaea were surveyed in an arid landfill using leachate collected from distinctly aged landfill cells (i.e., younger, intermediate, and older). We hypothesized that distinct methanogenic niches exist within an arid landfill, driven by geochemical gradients that developed under extended and age-dependent waste biodegradation stages. Using 16S rRNA and mcrA gene amplicon sequencing, we identified putative methanogenic niches as follows. The order Methanomicrobiales was the most abundant order in leachate from younger cells, where leachate temperature and propionate concentrations were measured at 41.8°C ± 1.7°C and 57.1 ± 10.7 mg L(−1). In intermediate-aged cells, the family Methanocellaceae was identified as a putative specialist family under intermediate-temperature and -total dissolved solid (TDS) conditions, wherein samples had a higher alpha diversity index and near CH(4) concentrations. In older-aged cells, accumulating metals and TDS supported Methanocorpusculaceae, “Candidatus Bathyarchaeota,” and “Candidatus Verstraetearchaeota” operational taxonomic units (OTUs). Consistent with the mcrA data, we assayed methanogenic activity across the age gradient through stable isotopic measurements of δ(13)C of CH(4) and δ(13)C of CO(2). The majority (80%) of the samples’ carbon fractionation was consistent with hydrogenotrophic methanogenesis. Together, we report age-dependent geochemical gradients detected through leachate in an arid landfill seemingly influencing CH(4) production, niche partitioning, and methanogenic activity. IMPORTANCE Microbiome analysis is becoming common in select municipal and service ecosystems, including wastewater treatment and anaerobic digestion, but its potential as a microbial-status-informative tool to promote or mitigate CH(4) production has not yet been evaluated in landfills. Methanogenesis mediated by Archaea is highly active in solid-waste microbiomes but is commonly neglected in studies employing next-generation sequencing techniques. Identifying methanogenic niches within a landfill offers detail into operations that positively or negatively impact the commercial production of methane known as biomethanation. We provide evidence that the geochemistry of leachate and its microbiome can be a variable accounting for ecosystem-level (coarse) variation of CH(4) production, where we demonstrate through independent assessments of leachate and gas collection that the functional variability of an arid landfill is linked to the composition of methanogenic Archaea. American Society for Microbiology 2022-04-11 /pmc/articles/PMC9088289/ /pubmed/35404071 http://dx.doi.org/10.1128/aem.02438-21 Text en Copyright © 2022 Reynolds et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Microbial Ecology
Reynolds, Mark C.
Finn, Damien
Sarno, Analissa F.
Allen, Richard
Deathrage, J. David
Krajmalnik-Brown, Rosa
Cadillo-Quiroz, Hinsby
Delineating the Drivers and Functionality of Methanogenic Niches within an Arid Landfill
title Delineating the Drivers and Functionality of Methanogenic Niches within an Arid Landfill
title_full Delineating the Drivers and Functionality of Methanogenic Niches within an Arid Landfill
title_fullStr Delineating the Drivers and Functionality of Methanogenic Niches within an Arid Landfill
title_full_unstemmed Delineating the Drivers and Functionality of Methanogenic Niches within an Arid Landfill
title_short Delineating the Drivers and Functionality of Methanogenic Niches within an Arid Landfill
title_sort delineating the drivers and functionality of methanogenic niches within an arid landfill
topic Microbial Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9088289/
https://www.ncbi.nlm.nih.gov/pubmed/35404071
http://dx.doi.org/10.1128/aem.02438-21
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