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Title: Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics

Abstract

Here we report that high-throughput sequencing is expanding our knowledge of microbial diversity in the environment. Still, understanding the metabolic potentials and ecological roles of rare and uncultured microbes in natural communities remains a major challenge. To this end, we applied a ‘divide and conquer’ strategy that partitioned a massive metagenomic data set (>100 Gbp) into subsets based on K-mer frequency in sequence assembly to a low-diversity acid mine drainage (AMD) microbial community and, by integrating with an additional metatranscriptomic assembly, successfully obtained 11 draft genomes most of which represent yet uncultured and/or rare taxa (relative abundance <1%). We report the first genome of a naturally occurring Ferrovum population (relative abundance >90%) and its metabolic potentials and gene expression profile, providing initial molecular insights into the ecological role of these lesser known, but potentially important, microorganisms in the AMD environment. Gene transcriptional analysis of the active taxa revealed major metabolic capabilities executed in situ, including carbon- and nitrogen-related metabolisms associated with syntrophic interactions, iron and sulfur oxidation, which are key in energy conservation and AMD generation, and the mechanisms of adaptation and response to the environmental stresses (heavy metals, low pH and oxidative stress). Remarkably, nitrogen fixation and sulfur oxidationmore » were performed by the rare taxa, indicating their critical roles in the overall functioning and assembly of the AMD community. Finally, our study demonstrates the potential of the ‘divide and conquer’ strategy in high-throughput sequencing data assembly for genome reconstruction and functional partitioning analysis of both dominant and rare species in natural microbial assemblages.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [1];  [1]
  1. Sun Yat-Sen Univ., Guangzhou, (China). School of Chemistry and Chemical Engineering. College of Ecology and Evolution
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE; National Natural Science Foundation of China (NSFC)
OSTI Identifier:
1263515
Grant/Contract Number:  
4093212; U1201233; 31370154
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 9; Journal Issue: 6; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Hua, Zheng-Shuang, Han, Yu-Jiao, Chen, Lin-Xing, Liu, Jun, Hu, Min, Li, Sheng-Jin, Kuang, Jia-Liang, Chain, Patrick SG, Huang, Li-Nan, and Shu, Wen-Sheng. Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics. United States: N. p., 2014. Web. doi:10.1038/ismej.2014.212.
Hua, Zheng-Shuang, Han, Yu-Jiao, Chen, Lin-Xing, Liu, Jun, Hu, Min, Li, Sheng-Jin, Kuang, Jia-Liang, Chain, Patrick SG, Huang, Li-Nan, & Shu, Wen-Sheng. Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics. United States. https://doi.org/10.1038/ismej.2014.212
Hua, Zheng-Shuang, Han, Yu-Jiao, Chen, Lin-Xing, Liu, Jun, Hu, Min, Li, Sheng-Jin, Kuang, Jia-Liang, Chain, Patrick SG, Huang, Li-Nan, and Shu, Wen-Sheng. Fri . "Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics". United States. https://doi.org/10.1038/ismej.2014.212. https://www.osti.gov/servlets/purl/1263515.
@article{osti_1263515,
title = {Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics},
author = {Hua, Zheng-Shuang and Han, Yu-Jiao and Chen, Lin-Xing and Liu, Jun and Hu, Min and Li, Sheng-Jin and Kuang, Jia-Liang and Chain, Patrick SG and Huang, Li-Nan and Shu, Wen-Sheng},
abstractNote = {Here we report that high-throughput sequencing is expanding our knowledge of microbial diversity in the environment. Still, understanding the metabolic potentials and ecological roles of rare and uncultured microbes in natural communities remains a major challenge. To this end, we applied a ‘divide and conquer’ strategy that partitioned a massive metagenomic data set (>100 Gbp) into subsets based on K-mer frequency in sequence assembly to a low-diversity acid mine drainage (AMD) microbial community and, by integrating with an additional metatranscriptomic assembly, successfully obtained 11 draft genomes most of which represent yet uncultured and/or rare taxa (relative abundance <1%). We report the first genome of a naturally occurring Ferrovum population (relative abundance >90%) and its metabolic potentials and gene expression profile, providing initial molecular insights into the ecological role of these lesser known, but potentially important, microorganisms in the AMD environment. Gene transcriptional analysis of the active taxa revealed major metabolic capabilities executed in situ, including carbon- and nitrogen-related metabolisms associated with syntrophic interactions, iron and sulfur oxidation, which are key in energy conservation and AMD generation, and the mechanisms of adaptation and response to the environmental stresses (heavy metals, low pH and oxidative stress). Remarkably, nitrogen fixation and sulfur oxidation were performed by the rare taxa, indicating their critical roles in the overall functioning and assembly of the AMD community. Finally, our study demonstrates the potential of the ‘divide and conquer’ strategy in high-throughput sequencing data assembly for genome reconstruction and functional partitioning analysis of both dominant and rare species in natural microbial assemblages.},
doi = {10.1038/ismej.2014.212},
journal = {The ISME Journal},
number = 6,
volume = 9,
place = {United States},
year = {Fri Nov 07 00:00:00 EST 2014},
month = {Fri Nov 07 00:00:00 EST 2014}
}

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  • DOI: 10.1111/1462-2920.13594

Recovering complete and draft population genomes from metagenome datasets
journal, March 2016


Stability of Cross-Feeding Polymorphisms in Microbial Communities
journal, December 2016


Microbial diversity and metabolic networks in acid mine drainage habitats
journal, May 2015

  • Méndez-García, Celia; Peláez, Ana I.; Mesa, Victoria
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00475

Gene Loss and Horizontal Gene Transfer Contributed to the Genome Evolution of the Extreme Acidophile “Ferrovum”
journal, May 2016

  • Ullrich, Sophie R.; González, Carolina; Poehlein, Anja
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00797

Microbial Community Shifts in Response to Acid Mine Drainage Pollution Within a Natural Wetland Ecosystem
journal, June 2018


Sulfur Oxidation in the Acidophilic Autotrophic Acidithiobacillus spp.
journal, January 2019


Microbial Diversity and Community Assembly across Environmental Gradients in Acid Mine Drainage
journal, June 2017

  • Teng, Wenkai; Kuang, Jialiang; Luo, Zhenhao
  • Minerals, Vol. 7, Issue 6, p. 106
  • DOI: 10.3390/min7060106

Comparative analysis of the rhizomicrobiome of the wild versus cultivated crop: insights from rice and soybean
journal, April 2019


Comparative Analyses of the Microbial Communities Inhabiting Coal Mining Waste Dump and an Adjacent Acid Mine Drainage Creek
journal, March 2019


Different Interspecies Electron Transfer Patterns during Mesophilic and Thermophilic Syntrophic Propionate Degradation in Chemostats
journal, January 2020


Influence of initial pH on bioleaching of river sediments to achieve deep dehydration
journal, April 2019

  • Shi, Mingyan; Wen, Guicheng; Liu, Hengfu
  • Environmental Science and Pollution Research, Vol. 26, Issue 17
  • DOI: 10.1007/s11356-019-04982-w

The potential of genomics for restoring ecosystems and biodiversity
journal, July 2019

  • Breed, Martin F.; Harrison, Peter A.; Blyth, Colette
  • Nature Reviews Genetics, Vol. 20, Issue 10
  • DOI: 10.1038/s41576-019-0152-0

Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
journal, September 2018

  • Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik
  • Nature Reviews Microbiology, Vol. 16, Issue 10
  • DOI: 10.1038/s41579-018-0076-2

The microbial genomics of arsenic
journal, January 2016

  • Andres, Jérémy; Bertin, Philippe N.
  • FEMS Microbiology Reviews, Vol. 40, Issue 2
  • DOI: 10.1093/femsre/fuv050

Recovering cellular biomass from fluids using chemical flocculation: Microbial cell flocs
journal, October 2018

  • Kenward, Paul A.; Simister, Rachel L.; Morgan-Lang, Connor
  • Environmental Microbiology Reports, Vol. 10, Issue 6
  • DOI: 10.1111/1758-2229.12690

Metagenome-scale analysis yields insights into the structure and function of microbial communities in a copper bioleaching heap
journal, January 2016


Comparative Genomics Unravels the Functional Roles of Co-occurring Acidophilic Bacteria in Bioleaching Heaps
journal, May 2017


The Inner Workings of the Outer Surface: Skin and Gill Microbiota as Indicators of Changing Gut Health in Yellowtail Kingfish
journal, January 2018

  • Legrand, Thibault P. R. A.; Catalano, Sarah R.; Wos-Oxley, Melissa L.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02664

Diversity of Prokaryotic Communities Indigenous to Acid Mine Drainage and Related Rocks from Baiyin Open-Pit Copper Mine Stope, China
journal, March 2018


Genomic signatures and co‐occurrence patterns of the ultra‐small Saccharimonadia (phylum CPR/Patescibacteria) suggest a symbiotic lifestyle
journal, September 2019

  • Lemos, Leandro N.; Medeiros, Julliane D.; Dini‐Andreote, Francisco
  • Molecular Ecology, Vol. 28, Issue 18
  • DOI: 10.1111/mec.15208

Where less may be more: how the rare biosphere pulls ecosystems strings
text, January 2017

  • Jousset, Alexandre; Rillig, Matthias C.; Bienhold, Christina
  • Freie Universität Berlin
  • DOI: 10.17169/refubium-25396

Composition of bacterial community in enrichment cultures of shale by-products from Irati Formation, Brazil
journal, October 2018

  • Goes, Kelly Campos Guerra Pinheiro de; Lovato, Gisele Milani; Andrade, Diva S.
  • Brazilian Journal of Microbiology, Vol. 49, Issue 4
  • DOI: 10.1016/j.bjm.2017.12.009

Capturing the genetic makeup of the active microbiome in situ
journal, June 2017

  • Singer, Esther; Wagner, Michael; Woyke, Tanja
  • The ISME Journal, Vol. 11, Issue 9
  • DOI: 10.1038/ismej.2017.59

Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems
journal, December 2019


Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota
journal, July 2018


Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea
journal, October 2019


Metagenome-scale analysis yields insights into the structure and function of microbial communities in a copper bioleaching heap
journal, January 2016


Recovering complete and draft population genomes from metagenome datasets
journal, March 2016


Diversity in a Polymicrobial Community Revealed by Analysis of Viromes, Endolysins and CRISPR Spacers
journal, September 2016


Microbial diversity and metabolic networks in acid mine drainage habitats
journal, May 2015

  • Méndez-García, Celia; Peláez, Ana I.; Mesa, Victoria
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00475

Gene Loss and Horizontal Gene Transfer Contributed to the Genome Evolution of the Extreme Acidophile “Ferrovum”
journal, May 2016

  • Ullrich, Sophie R.; González, Carolina; Poehlein, Anja
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00797

Comparative Genomics Unravels the Functional Roles of Co-occurring Acidophilic Bacteria in Bioleaching Heaps
journal, May 2017


Unexpected Dominance of Elusive Acidobacteria in Early Industrial Soft Coal Slags
journal, June 2017


Bacterial, Archaeal, and Eukaryotic Diversity across Distinct Microhabitats in an Acid Mine Drainage
journal, September 2017

  • Mesa, Victoria; Gallego, Jose L. R.; González-Gil, Ricardo
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01756

The Inner Workings of the Outer Surface: Skin and Gill Microbiota as Indicators of Changing Gut Health in Yellowtail Kingfish
journal, January 2018

  • Legrand, Thibault P. R. A.; Catalano, Sarah R.; Wos-Oxley, Melissa L.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02664