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Title: Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage

Abstract

The ecosystem roles of fungi have been extensively studied by targeting one organism and/or biological process at a time, but the full metabolic potential of fungi has rarely been captured in an environmental context. We hypothesized that fungal genome sequences could be assembled directly from the environment using metagenomics and that transcriptomics and proteomics could simultaneously reveal metabolic differentiation across habitats. We reconstructed the near-complete 27 Mbp genome of a filamentous fungus, Acidomyces richmondensis, and evaluated transcript and protein expression in floating and streamer biofilms from an acid mine drainage (AMD) system. A. richmondensis transcripts involved in denitrification and in the degradation of complex carbon sources (including cellulose) were up-regulated in floating biofilms, whereas central carbon metabolism and stress-related transcripts were significantly up-regulated in streamer biofilms. Finally, these findings suggest that the biofilm niches are distinguished by distinct carbon and nitrogen resource utilization, oxygen availability, and environmental challenges. An isolated A. richmondensis strain from this environment was used to validate the metagenomics-derived genome and confirm nitrous oxide production at pH 1. Overall, our analyses defined mechanisms of fungal adaptation and identified a functional shift related to different roles in carbon and nitrogen turnover for the same species of fungi growingmore » in closely located but distinct biofilm niches.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [2];  [2];  [2];  [2];  [2];  [2];  [3];  [3];  [2];  [4];  [1]
  1. Univ. of California, Berkeley, CA (United States)
  2. US Dept. of Energy Joint Genome Institute, Walnut Creek, CA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1257271
Alternate Identifier(s):
OSTI ID: 1326500; OSTI ID: 1379136
Grant/Contract Number:  
FG02-10ER64996; SC0004918; AC02-05CH11231; AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; fungi; metagenomics; transcriptomics; proteomics; carbon; nitrogen; biofilm

Citation Formats

Mosier, Annika C., Miller, Christopher S., Frischkorn, Kyle R., Ohm, Robin A., Li, Zhou, LaButti, Kurt, Lapidus, Alla, Lipzen, Anna, Chen, Cindy, Johnson, Jenifer, Lindquist, Erika A., Pan, Chongle, Hettich, Robert L., Grigoriev, Igor V., Singer, Steven W., and Banfield, Jillian F. Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00238.
Mosier, Annika C., Miller, Christopher S., Frischkorn, Kyle R., Ohm, Robin A., Li, Zhou, LaButti, Kurt, Lapidus, Alla, Lipzen, Anna, Chen, Cindy, Johnson, Jenifer, Lindquist, Erika A., Pan, Chongle, Hettich, Robert L., Grigoriev, Igor V., Singer, Steven W., & Banfield, Jillian F. Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage. United States. doi:10.3389/fmicb.2016.00238.
Mosier, Annika C., Miller, Christopher S., Frischkorn, Kyle R., Ohm, Robin A., Li, Zhou, LaButti, Kurt, Lapidus, Alla, Lipzen, Anna, Chen, Cindy, Johnson, Jenifer, Lindquist, Erika A., Pan, Chongle, Hettich, Robert L., Grigoriev, Igor V., Singer, Steven W., and Banfield, Jillian F. Thu . "Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage". United States. doi:10.3389/fmicb.2016.00238. https://www.osti.gov/servlets/purl/1257271.
@article{osti_1257271,
title = {Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage},
author = {Mosier, Annika C. and Miller, Christopher S. and Frischkorn, Kyle R. and Ohm, Robin A. and Li, Zhou and LaButti, Kurt and Lapidus, Alla and Lipzen, Anna and Chen, Cindy and Johnson, Jenifer and Lindquist, Erika A. and Pan, Chongle and Hettich, Robert L. and Grigoriev, Igor V. and Singer, Steven W. and Banfield, Jillian F.},
abstractNote = {The ecosystem roles of fungi have been extensively studied by targeting one organism and/or biological process at a time, but the full metabolic potential of fungi has rarely been captured in an environmental context. We hypothesized that fungal genome sequences could be assembled directly from the environment using metagenomics and that transcriptomics and proteomics could simultaneously reveal metabolic differentiation across habitats. We reconstructed the near-complete 27 Mbp genome of a filamentous fungus, Acidomyces richmondensis, and evaluated transcript and protein expression in floating and streamer biofilms from an acid mine drainage (AMD) system. A. richmondensis transcripts involved in denitrification and in the degradation of complex carbon sources (including cellulose) were up-regulated in floating biofilms, whereas central carbon metabolism and stress-related transcripts were significantly up-regulated in streamer biofilms. Finally, these findings suggest that the biofilm niches are distinguished by distinct carbon and nitrogen resource utilization, oxygen availability, and environmental challenges. An isolated A. richmondensis strain from this environment was used to validate the metagenomics-derived genome and confirm nitrous oxide production at pH 1. Overall, our analyses defined mechanisms of fungal adaptation and identified a functional shift related to different roles in carbon and nitrogen turnover for the same species of fungi growing in closely located but distinct biofilm niches.},
doi = {10.3389/fmicb.2016.00238},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {Thu Mar 03 00:00:00 EST 2016},
month = {Thu Mar 03 00:00:00 EST 2016}
}

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Cited by: 5 works
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