Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem

ABSTRACT The geological role of microorganisms has been widely studied in the karst cave ecosystem. However, microbial interactions and ecological functions in such a dark, humid, and oligotrophic habitat have received far less attention, which is crucial to understanding cave biogeochemistry. Herei...

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Main Authors: Liyuan Ma, Xinping Huang, Hongmei Wang, Yuan Yun, Xiaoyu Cheng, Deng Liu, Xiaolu Lu, Xuan Qiu
Format: Article
Language:English
Published: American Society for Microbiology 2021-10-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/Spectrum.01152-21
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author Liyuan Ma
Xinping Huang
Hongmei Wang
Yuan Yun
Xiaoyu Cheng
Deng Liu
Xiaolu Lu
Xuan Qiu
author_facet Liyuan Ma
Xinping Huang
Hongmei Wang
Yuan Yun
Xiaoyu Cheng
Deng Liu
Xiaolu Lu
Xuan Qiu
author_sort Liyuan Ma
collection DOAJ
description ABSTRACT The geological role of microorganisms has been widely studied in the karst cave ecosystem. However, microbial interactions and ecological functions in such a dark, humid, and oligotrophic habitat have received far less attention, which is crucial to understanding cave biogeochemistry. Herein, microorganisms from weathered rock and sediment along the Heshang Cave depth were analyzed by random matrix theory-based network and Tax4Fun functional prediction. The results showed that although the cave microbial communities have spatial heterogeneity, differential habitats drove the community structure and diversity. Actinobacteria were predominant in weathered rock, whereas Proteobacteria dominated the sediment. The sediment communities presented significantly higher alpha diversities due to the relatively abundant nutrition from the outside by the intermittent stream. Consistently, microbial interactions in sediment were more complex, as visualized by more nodes and links. The abundant taxa presented more positive correlations with other community members in both of the two networks, indicating that they relied on promotion effects to adapt to the extreme environment. The keystones in weathered rock were mainly involved in the biodegradation of organic compounds, whereas the keystone Nitrospira in sediment contributed to carbon/nitrogen fixation. Collectively, these findings suggest that microbial interactions may lead to distinct taxonomic and functional communities in weathered rock and sediment in the subsurface Heshang Cave. IMPORTANCE In general, the constant physicochemical conditions and limited nutrient sources over long periods in the subsurface support a stable ecosystem in karst cave. Previous studies on cave microbial ecology were mostly focused on community composition, diversity, and the relationship with local environmental factors. There are still many unknowns about the microbial interactions and functions in such a dark environment with little human interference. Two representative habitats, including weathered rock and sediment in Heshang Cave, were selected to give an integrated insight into microbial interactions and potential functions. The cooccurrence network, especially the subnetwork, was used to characterize the cave microbial interactions in detail. We demonstrated that abundant taxa primarily relied on promotion effects rather than inhibition effects to survive in Heshang Cave. Keystone species may play important metabolic roles in sustaining ecological functions. Our study provides improved understanding of microbial interaction patterns and community ecological functions in the karst cave ecosystem.
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spelling doaj.art-b0795fb3d29f4186b9455948785082842022-12-21T21:19:22ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972021-10-019210.1128/Spectrum.01152-21Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave EcosystemLiyuan Ma0Xinping Huang1Hongmei Wang2Yuan Yun3Xiaoyu Cheng4Deng Liu5Xiaolu Lu6Xuan Qiu7School of Environmental Studies, China University of Geosciences, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences, Wuhan, ChinaState Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan, ChinaABSTRACT The geological role of microorganisms has been widely studied in the karst cave ecosystem. However, microbial interactions and ecological functions in such a dark, humid, and oligotrophic habitat have received far less attention, which is crucial to understanding cave biogeochemistry. Herein, microorganisms from weathered rock and sediment along the Heshang Cave depth were analyzed by random matrix theory-based network and Tax4Fun functional prediction. The results showed that although the cave microbial communities have spatial heterogeneity, differential habitats drove the community structure and diversity. Actinobacteria were predominant in weathered rock, whereas Proteobacteria dominated the sediment. The sediment communities presented significantly higher alpha diversities due to the relatively abundant nutrition from the outside by the intermittent stream. Consistently, microbial interactions in sediment were more complex, as visualized by more nodes and links. The abundant taxa presented more positive correlations with other community members in both of the two networks, indicating that they relied on promotion effects to adapt to the extreme environment. The keystones in weathered rock were mainly involved in the biodegradation of organic compounds, whereas the keystone Nitrospira in sediment contributed to carbon/nitrogen fixation. Collectively, these findings suggest that microbial interactions may lead to distinct taxonomic and functional communities in weathered rock and sediment in the subsurface Heshang Cave. IMPORTANCE In general, the constant physicochemical conditions and limited nutrient sources over long periods in the subsurface support a stable ecosystem in karst cave. Previous studies on cave microbial ecology were mostly focused on community composition, diversity, and the relationship with local environmental factors. There are still many unknowns about the microbial interactions and functions in such a dark environment with little human interference. Two representative habitats, including weathered rock and sediment in Heshang Cave, were selected to give an integrated insight into microbial interactions and potential functions. The cooccurrence network, especially the subnetwork, was used to characterize the cave microbial interactions in detail. We demonstrated that abundant taxa primarily relied on promotion effects rather than inhibition effects to survive in Heshang Cave. Keystone species may play important metabolic roles in sustaining ecological functions. Our study provides improved understanding of microbial interaction patterns and community ecological functions in the karst cave ecosystem.https://journals.asm.org/doi/10.1128/Spectrum.01152-21cooccurrence networkfunctional predictionkarst cavekeystone speciesmicrobial interactions
spellingShingle Liyuan Ma
Xinping Huang
Hongmei Wang
Yuan Yun
Xiaoyu Cheng
Deng Liu
Xiaolu Lu
Xuan Qiu
Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem
Microbiology Spectrum
cooccurrence network
functional prediction
karst cave
keystone species
microbial interactions
title Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem
title_full Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem
title_fullStr Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem
title_full_unstemmed Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem
title_short Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem
title_sort microbial interactions drive distinct taxonomic and potential metabolic responses to habitats in karst cave ecosystem
topic cooccurrence network
functional prediction
karst cave
keystone species
microbial interactions
url https://journals.asm.org/doi/10.1128/Spectrum.01152-21
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