Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake
Background Microbial processes are intricately linked to the depletion of oxygen in in-land and coastal water bodies, with devastating economic and ecological consequences. Microorganisms deplete oxygen during biomass decomposition, degrading the habitat of many economically importa...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BioMed Central
2018
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| Online Access: | http://hdl.handle.net/1721.1/118194 https://orcid.org/0000-0001-5400-4945 https://orcid.org/0000-0002-6684-6426 https://orcid.org/0000-0002-5981-2500 https://orcid.org/0000-0002-2744-8994 |
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| author | Arora-Williams, Keith Abraham, Sonali Sooklal, Alyssa Preheim, Sarah P Olesen, Scott W. Scandella, Benjamin P. Spencer, Sarah J. Myers, Elise M. Preheim, Sarah P. Olesen, Scott Wilder Scandella, Benjamin Delwiche, Kyle Brook Myers, Elise McKenna |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Arora-Williams, Keith Abraham, Sonali Sooklal, Alyssa Preheim, Sarah P Olesen, Scott W. Scandella, Benjamin P. Spencer, Sarah J. Myers, Elise M. Preheim, Sarah P. Olesen, Scott Wilder Scandella, Benjamin Delwiche, Kyle Brook Myers, Elise McKenna |
| author_sort | Arora-Williams, Keith |
| collection | MIT |
| description | Background
Microbial processes are intricately linked to the depletion of oxygen in in-land and coastal water bodies, with devastating economic and ecological consequences. Microorganisms deplete oxygen during biomass decomposition, degrading the habitat of many economically important aquatic animals. Microbes then turn to alternative electron acceptors, which alter nutrient cycling and generate potent greenhouse gases. As oxygen depletion is expected to worsen with altered land use and climate change, understanding how chemical and microbial dynamics impact dead zones will aid modeling efforts to guide remediation strategies. More work is needed to understand the complex interplay between microbial genes, populations, and biogeochemistry during oxygen depletion.
Results
Here, we used 16S rRNA gene surveys, shotgun metagenomic sequencing, and a previously developed biogeochemical model to identify genes and microbial populations implicated in major biogeochemical transformations in a model lake ecosystem. Shotgun metagenomic sequencing was done for one time point in Aug., 2013, and 16S rRNA gene sequencing was done for a 5-month time series (Mar.–Aug., 2013) to capture the spatiotemporal dynamics of genes and microorganisms mediating the modeled processes. Metagenomic binning analysis resulted in many metagenome-assembled genomes (MAGs) that are implicated in the modeled processes through gene content similarity to cultured organism and the presence of key genes involved in these pathways. The MAGs suggested some populations are capable of methane and sulfide oxidation coupled to nitrate reduction. Using the model, we observe that modulating these processes has a substantial impact on overall lake biogeochemistry. Additionally, 16S rRNA gene sequences from the metagenomic and amplicon libraries were linked to processes through the MAGs. We compared the dynamics of microbial populations in the water column to the model predictions. Many microbial populations involved in primary carbon oxidation had dynamics similar to the model, while those associated with secondary oxidation processes deviated substantially.
Conclusions
This work demonstrates that the unique capabilities of resident microbial populations will substantially impact the concentration and speciation of chemicals in the water column, unless other microbial processes adjust to compensate for these differences. It further highlights the importance of the biological aspects of biogeochemical processes, such as fluctuations in microbial population dynamics. Integrating gene and population dynamics into biogeochemical models has the potential to improve predictions of the community response under altered scenarios to guide remediation efforts. |
| first_indexed | 2024-09-23T11:25:09Z |
| format | Article |
| id | mit-1721.1/118194 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T11:25:09Z |
| publishDate | 2018 |
| publisher | BioMed Central |
| record_format | dspace |
| spelling | mit-1721.1/1181942022-09-27T19:25:59Z Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake Arora-Williams, Keith Abraham, Sonali Sooklal, Alyssa Preheim, Sarah P Olesen, Scott W. Scandella, Benjamin P. Spencer, Sarah J. Myers, Elise M. Preheim, Sarah P. Olesen, Scott Wilder Scandella, Benjamin Delwiche, Kyle Brook Myers, Elise McKenna Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Olesen, Scott Wilder Scandella, Benjamin Delwiche, Kyle Brook Spencer, Sarah J. Myers, Elise McKenna Background Microbial processes are intricately linked to the depletion of oxygen in in-land and coastal water bodies, with devastating economic and ecological consequences. Microorganisms deplete oxygen during biomass decomposition, degrading the habitat of many economically important aquatic animals. Microbes then turn to alternative electron acceptors, which alter nutrient cycling and generate potent greenhouse gases. As oxygen depletion is expected to worsen with altered land use and climate change, understanding how chemical and microbial dynamics impact dead zones will aid modeling efforts to guide remediation strategies. More work is needed to understand the complex interplay between microbial genes, populations, and biogeochemistry during oxygen depletion. Results Here, we used 16S rRNA gene surveys, shotgun metagenomic sequencing, and a previously developed biogeochemical model to identify genes and microbial populations implicated in major biogeochemical transformations in a model lake ecosystem. Shotgun metagenomic sequencing was done for one time point in Aug., 2013, and 16S rRNA gene sequencing was done for a 5-month time series (Mar.–Aug., 2013) to capture the spatiotemporal dynamics of genes and microorganisms mediating the modeled processes. Metagenomic binning analysis resulted in many metagenome-assembled genomes (MAGs) that are implicated in the modeled processes through gene content similarity to cultured organism and the presence of key genes involved in these pathways. The MAGs suggested some populations are capable of methane and sulfide oxidation coupled to nitrate reduction. Using the model, we observe that modulating these processes has a substantial impact on overall lake biogeochemistry. Additionally, 16S rRNA gene sequences from the metagenomic and amplicon libraries were linked to processes through the MAGs. We compared the dynamics of microbial populations in the water column to the model predictions. Many microbial populations involved in primary carbon oxidation had dynamics similar to the model, while those associated with secondary oxidation processes deviated substantially. Conclusions This work demonstrates that the unique capabilities of resident microbial populations will substantially impact the concentration and speciation of chemicals in the water column, unless other microbial processes adjust to compensate for these differences. It further highlights the importance of the biological aspects of biogeochemical processes, such as fluctuations in microbial population dynamics. Integrating gene and population dynamics into biogeochemical models has the potential to improve predictions of the community response under altered scenarios to guide remediation efforts. 2018-09-28T16:02:21Z 2018-09-28T16:02:21Z 2018-09 2018-05 2018-09-23T03:32:16Z Article http://purl.org/eprint/type/JournalArticle 2049-2618 http://hdl.handle.net/1721.1/118194 Arora-Williams, Keith et al. "Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake." Microbiome 6 (September 2018): 165 © 2018 The Authors https://orcid.org/0000-0001-5400-4945 https://orcid.org/0000-0002-6684-6426 https://orcid.org/0000-0002-5981-2500 https://orcid.org/0000-0002-2744-8994 en https://doi.org/10.1186/s40168-018-0556-7 Microbiome Creative Commons Attribution http://creativecommons.org/licenses/by/4.0/ The Author(s). application/pdf BioMed Central BioMed Central |
| spellingShingle | Arora-Williams, Keith Abraham, Sonali Sooklal, Alyssa Preheim, Sarah P Olesen, Scott W. Scandella, Benjamin P. Spencer, Sarah J. Myers, Elise M. Preheim, Sarah P. Olesen, Scott Wilder Scandella, Benjamin Delwiche, Kyle Brook Myers, Elise McKenna Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake |
| title | Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake |
| title_full | Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake |
| title_fullStr | Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake |
| title_full_unstemmed | Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake |
| title_short | Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake |
| title_sort | dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake |
| url | http://hdl.handle.net/1721.1/118194 https://orcid.org/0000-0001-5400-4945 https://orcid.org/0000-0002-6684-6426 https://orcid.org/0000-0002-5981-2500 https://orcid.org/0000-0002-2744-8994 |
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