Contrasting prokaryotic and eukaryotic community assembly and species coexistence in acid mine drainage-polluted waters

Acid mine drainage (AMD) is characterized by high acidity and high-concentration metals and sulfate, representing an extreme environment to life as well as environmental challenge worldwide. Microorganisms thriving in AMD habitats have evolved with distinct mechanisms in response to multiple stresse...

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Published inThe Science of the total environment Vol. 856; p. 158954
Main Authors She, Zhixiang, Pan, Xin, Yue, Zhengbo, Shi, Xiufeng, Gao, Yijun, Wang, Shaoping, Chuai, Xin, Wang, Jin
Format Journal Article
LanguageEnglish
Published Elsevier B.V 15.01.2023
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Abstract Acid mine drainage (AMD) is characterized by high acidity and high-concentration metals and sulfate, representing an extreme environment to life as well as environmental challenge worldwide. Microorganisms thriving in AMD habitats have evolved with distinct mechanisms in response to multiple stresses. Compared with microbial prokaryotes, our understanding regarding eukaryotic occurrence and role in AMD habitats remain limited. Here we examined microbial diversity and co-occurrence pattern within all domains of life in five lakes with varying degrees of AMD contamination ranging from extremely acidic to neutral. We demonstrated that AMD pollution reduced both eukaryotic and prokaryotic diversity in the lakes. In lakes with serious AMD pollution, chemoautotrophs including Ferrovum, Acidithiobacillus, and Leptospirillum showed significantly higher abundance, whereas with the macroscopic growths of photosynthetic microalgae (e.g., Coccomyxa and Chlamydomonas), heterotrophic or mixotrophic prokaryotes (e.g., Acidiphilium, Thiomonas, and Alicyclobacillus) increased in less polluted lakes. In the further improved ecosystems, Ochromonas, Rotifer, Ciliophora and other microeukaryotes appeared. Combined with a public dataset focusing on the microbes along an AMD-contaminated stream, we further demonstrated that acidity-dominated environmental selection served as the primary driver of both eukaryotic and prokaryotic community assemblies, and to a greater extent for eukaryotes. Furthermore, specific prokaryotic and eukaryotic taxa (e.g., Proteobacteria and Chlorophyta) exhibited wide taxonomic and functional associations in these AMD-polluted waters. These findings expand our knowledge on the eukaryotic diversity in AMD habitats, and provide insights into the ecological processes underlying microbial communities in response to AMD contamination. [Display omitted] •Prokaryotes and eukaryotes covary along AMD-induced environmental gradients.•Eukaryotic microorganisms are more sensitive to AMD-induced environmental stress.•The pH determines the diversity and distribution of both eukaryotes and prokaryotes.•Specific taxa (e.g., Proteobacteria and Chlorophyta) have interkingdom connections.
AbstractList Acid mine drainage (AMD) is characterized by high acidity and high-concentration metals and sulfate, representing an extreme environment to life as well as environmental challenge worldwide. Microorganisms thriving in AMD habitats have evolved with distinct mechanisms in response to multiple stresses. Compared with microbial prokaryotes, our understanding regarding eukaryotic occurrence and role in AMD habitats remain limited. Here we examined microbial diversity and co-occurrence pattern within all domains of life in five lakes with varying degrees of AMD contamination ranging from extremely acidic to neutral. We demonstrated that AMD pollution reduced both eukaryotic and prokaryotic diversity in the lakes. In lakes with serious AMD pollution, chemoautotrophs including Ferrovum, Acidithiobacillus, and Leptospirillum showed significantly higher abundance, whereas with the macroscopic growths of photosynthetic microalgae (e.g., Coccomyxa and Chlamydomonas), heterotrophic or mixotrophic prokaryotes (e.g., Acidiphilium, Thiomonas, and Alicyclobacillus) increased in less polluted lakes. In the further improved ecosystems, Ochromonas, Rotifer, Ciliophora and other microeukaryotes appeared. Combined with a public dataset focusing on the microbes along an AMD-contaminated stream, we further demonstrated that acidity-dominated environmental selection served as the primary driver of both eukaryotic and prokaryotic community assemblies, and to a greater extent for eukaryotes. Furthermore, specific prokaryotic and eukaryotic taxa (e.g., Proteobacteria and Chlorophyta) exhibited wide taxonomic and functional associations in these AMD-polluted waters. These findings expand our knowledge on the eukaryotic diversity in AMD habitats, and provide insights into the ecological processes underlying microbial communities in response to AMD contamination. [Display omitted] •Prokaryotes and eukaryotes covary along AMD-induced environmental gradients.•Eukaryotic microorganisms are more sensitive to AMD-induced environmental stress.•The pH determines the diversity and distribution of both eukaryotes and prokaryotes.•Specific taxa (e.g., Proteobacteria and Chlorophyta) have interkingdom connections.
ArticleNumber 158954
Author Chuai, Xin
Yue, Zhengbo
Pan, Xin
Wang, Shaoping
Wang, Jin
Gao, Yijun
She, Zhixiang
Shi, Xiufeng
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  givenname: Shaoping
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  givenname: Jin
  surname: Wang
  fullname: Wang, Jin
  email: sophiawj@hfut.edu.cn
  organization: School of Resources and Environmental Engineering, Hefei University of Technology, Hefei, Anhui 230009, China
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Keywords Microeukaryote
Community assembly
Acid mine drainage
Co-occurrence
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Environmental gradient
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Snippet Acid mine drainage (AMD) is characterized by high acidity and high-concentration metals and sulfate, representing an extreme environment to life as well as...
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StartPage 158954
SubjectTerms Acid mine drainage
Co-occurrence
Community assembly
Environmental gradient
Microbial community
Microeukaryote
Title Contrasting prokaryotic and eukaryotic community assembly and species coexistence in acid mine drainage-polluted waters
URI https://dx.doi.org/10.1016/j.scitotenv.2022.158954
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