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

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.

doi:10.3389/fmicb.2016.00238

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

Journal Article · Thu Mar 03 00:00:00 EST 2016 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2016.00238· OSTI ID:1257271

Mosier, Annika C. ^[1]; Miller, Christopher S. ^[1]; Frischkorn, Kyle R. ^[1]; Ohm, Robin A. ^[2]; Li, Zhou ^[3]; LaButti, Kurt ^[2]; Lapidus, Alla ^[2]; Lipzen, Anna ^[2]; Chen, Cindy ^[2]; Johnson, Jenifer ^[2]; Lindquist, Erika A. ^[2]; Pan, Chongle ^[3]; Hettich, Robert L. ^[3]; Grigoriev, Igor V. ^[2]; Singer, Steven W. ^[4]; Banfield, Jillian F. ^[1]

Univ. of California, Berkeley, CA (United States)
US Dept. of Energy Joint Genome Institute, Walnut Creek, CA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

© 2016 Mosier, Miller, Frischkorn, Ohm, Li, LaButti, Lapidus, Lipzen, Chen, Johnson, Lindquist, Pan, Hettich, Grigoriev, Singer and Banfield. 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. 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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FG02-10ER64996; SC0004918; AC02-05CH11231; AC05-00OR22725

OSTI ID:: 1257271

Alternate ID(s):: OSTI ID: 1326500; OSTI ID: 1379136

Journal Information:: Frontiers in Microbiology, Vol. 7; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 36 works

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Acidomyces acidophilus: Ecology, Biochemical Properties and Application to Bioremediation Chan, Wai Kit; Wildeboer, Dirk; Garelick, Hemda Fungi in Extreme Environments: Ecological Role and Biotechnological Significance, p. 505-515 https://doi.org/10.1007/978-3-030-19030-9_25	book	July 2019
Community Composition of Nitrite Reductase Gene Sequences in an Acid Mine Drainage Environment Wise, Ben R.; Roane, Timberley M.; Mosier, Annika C. Microbial Ecology, Vol. 79, Issue 3 https://doi.org/10.1007/s00248-019-01420-9	journal	August 2019
Interactions among microfungi and pyrite-chalcopyrite mineralizations: tolerance, mineral bioleaching, and metal bioaccumulation Cecchi, Grazia; Ceci, Andrea; Marescotti, Pietro Mycological Progress, Vol. 18, Issue 3 https://doi.org/10.1007/s11557-018-01466-y	journal	March 2019
The genome of opportunistic fungal pathogen Fusarium oxysporum carries a unique set of lineage-specific chromosomes Zhang, Yong; Yang, He; Turra, David Communications Biology, Vol. 3, Issue 1 https://doi.org/10.1038/s42003-020-0770-2	journal	January 2020
Genome Sequence of the Extremely Acidophilic Fungus Acidomyces richmondensis FRIK2901 Rosienski, Matthew D.; Lee, Mi-Kyung; Yu, Jae-Hyuk Microbiology Resource Announcements, Vol. 7, Issue 16 https://doi.org/10.1128/mra.01314-18	journal	October 2018
New insights on unspecific peroxygenases: superfamily reclassification and evolution Faiza, Muniba; Huang, Shengfeng; Lan, Dongming BMC Evolutionary Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12862-019-1394-3	journal	March 2019
Genome-scale data resolve ancestral rock-inhabiting lifestyle in Dothideomycetes (Ascomycota) Ametrano, Claudio G.; Grewe, Felix; Crous, Pedro W. IMA Fungus, Vol. 10, Issue 1 https://doi.org/10.1186/s43008-019-0018-2	journal	October 2019
Hiding in plain sight: New virus genomes discovered via a systematic analysis of fungal public transcriptomes Gilbert, Kerrigan B.; Holcomb, Emily E.; Allscheid, Robyn L. PLOS ONE, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pone.0219207	journal	July 2019
Comparative Genomics Unravels the Functional Roles of Co-occurring Acidophilic Bacteria in Bioleaching Heaps Zhang, Xian; Liu, Xueduan; Liang, Yili Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00790	journal	May 2017

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59 BASIC BIOLOGICAL SCIENCES
fungi
metagenomics
transcriptomics
proteomics
carbon
nitrogen
biofilm

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

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