Cargando…

Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments

BACKGROUND: Freshwater sediment microbes are crucial decomposers that play a key role in regulating biogeochemical cycles and greenhouse gas emissions. They often exhibit a highly ordered structure along depth profiles. This stratification not only reflects redox effects but also provides valuable i...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhou, Xiaotian, Lennon, Jay T., Lu, Xiang, Ruan, Aidong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10464086/
https://www.ncbi.nlm.nih.gov/pubmed/37626433
http://dx.doi.org/10.1186/s40168-023-01612-z
_version_ 1785098386366529536
author Zhou, Xiaotian
Lennon, Jay T.
Lu, Xiang
Ruan, Aidong
author_facet Zhou, Xiaotian
Lennon, Jay T.
Lu, Xiang
Ruan, Aidong
author_sort Zhou, Xiaotian
collection PubMed
description BACKGROUND: Freshwater sediment microbes are crucial decomposers that play a key role in regulating biogeochemical cycles and greenhouse gas emissions. They often exhibit a highly ordered structure along depth profiles. This stratification not only reflects redox effects but also provides valuable insights into historical transitions, as sediments serve as important archives for tracing environmental history. The Anthropocene, a candidate geological epoch, has recently garnered significant attention. However, the human impact on sediment zonation under the cover of natural redox niches remains poorly understood. Dam construction stands as one of the most far-reaching anthropogenic modifications of aquatic ecosystems. Here we attempted to identify the ecological imprint of damming on freshwater sediment microbiome. RESULTS: We conducted a year-round survey on the sediment profiles of Lake Chaohu, a large shallow lake in China. Through depth-discrete shotgun metagenomics, metataxonomics, and geophysiochemical analyses, we unveiled a unique prokaryotic hierarchy shaped by the interplay of redox regime and historical damming (labeled by the (137)Cs peak in AD 1963). Dam-induced initial differentiation was further amplified by nitrogen and methane metabolism, forming an abrupt transition governing nitrate–methane metabolic interaction and gaseous methane sequestration depth. Using a random forest algorithm, we identified damming-sensitive taxa that possess distinctive metabolic strategies, including energy-saving mechanisms, unique motility behavior, and deep-environment preferences. Moreover, null model analysis showed that damming altered microbial community assembly, from a selection-oriented deterministic process above to a more stochastic, dispersal-limited one below. Temporal investigation unveiled the rapid transition zone as an ecotone, characterized by high species richness, low community stability, and emergent stochasticity. Path analysis revealed the observed emergent stochasticity primarily came from the high metabolic flexibility, which potentially contributed to both ecological and statistical neutralities. CONCLUSIONS: We delineate a picture in which dam-induced modifications in nutrient availability and sedimentation rates impact microbial metabolic activities and generate great changes in the community structure, assembly, and stability of the freshwater sediment microbiome. These findings reflect profound ecological and biogeochemical ramifications of human–Earth system interactions and help re-examine the mainstream views on the formation of sediment microbial stratification. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01612-z.
format Online
Article
Text
id pubmed-10464086
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-104640862023-08-30 Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments Zhou, Xiaotian Lennon, Jay T. Lu, Xiang Ruan, Aidong Microbiome Research BACKGROUND: Freshwater sediment microbes are crucial decomposers that play a key role in regulating biogeochemical cycles and greenhouse gas emissions. They often exhibit a highly ordered structure along depth profiles. This stratification not only reflects redox effects but also provides valuable insights into historical transitions, as sediments serve as important archives for tracing environmental history. The Anthropocene, a candidate geological epoch, has recently garnered significant attention. However, the human impact on sediment zonation under the cover of natural redox niches remains poorly understood. Dam construction stands as one of the most far-reaching anthropogenic modifications of aquatic ecosystems. Here we attempted to identify the ecological imprint of damming on freshwater sediment microbiome. RESULTS: We conducted a year-round survey on the sediment profiles of Lake Chaohu, a large shallow lake in China. Through depth-discrete shotgun metagenomics, metataxonomics, and geophysiochemical analyses, we unveiled a unique prokaryotic hierarchy shaped by the interplay of redox regime and historical damming (labeled by the (137)Cs peak in AD 1963). Dam-induced initial differentiation was further amplified by nitrogen and methane metabolism, forming an abrupt transition governing nitrate–methane metabolic interaction and gaseous methane sequestration depth. Using a random forest algorithm, we identified damming-sensitive taxa that possess distinctive metabolic strategies, including energy-saving mechanisms, unique motility behavior, and deep-environment preferences. Moreover, null model analysis showed that damming altered microbial community assembly, from a selection-oriented deterministic process above to a more stochastic, dispersal-limited one below. Temporal investigation unveiled the rapid transition zone as an ecotone, characterized by high species richness, low community stability, and emergent stochasticity. Path analysis revealed the observed emergent stochasticity primarily came from the high metabolic flexibility, which potentially contributed to both ecological and statistical neutralities. CONCLUSIONS: We delineate a picture in which dam-induced modifications in nutrient availability and sedimentation rates impact microbial metabolic activities and generate great changes in the community structure, assembly, and stability of the freshwater sediment microbiome. These findings reflect profound ecological and biogeochemical ramifications of human–Earth system interactions and help re-examine the mainstream views on the formation of sediment microbial stratification. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01612-z. BioMed Central 2023-08-26 /pmc/articles/PMC10464086/ /pubmed/37626433 http://dx.doi.org/10.1186/s40168-023-01612-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zhou, Xiaotian
Lennon, Jay T.
Lu, Xiang
Ruan, Aidong
Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments
title Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments
title_full Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments
title_fullStr Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments
title_full_unstemmed Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments
title_short Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments
title_sort anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10464086/
https://www.ncbi.nlm.nih.gov/pubmed/37626433
http://dx.doi.org/10.1186/s40168-023-01612-z
work_keys_str_mv AT zhouxiaotian anthropogenicactivitiesmediatestratificationandstabilityofmicrobialcommunitiesinfreshwatersediments
AT lennonjayt anthropogenicactivitiesmediatestratificationandstabilityofmicrobialcommunitiesinfreshwatersediments
AT luxiang anthropogenicactivitiesmediatestratificationandstabilityofmicrobialcommunitiesinfreshwatersediments
AT ruanaidong anthropogenicactivitiesmediatestratificationandstabilityofmicrobialcommunitiesinfreshwatersediments