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. 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.
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley Berkeley, CA, USA.
authors.forename: Annika C
authors.initials: AC
authors.lastname: Mosier
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley Berkeley, CA, USA.
authors.forename: Christopher S
authors.initials: CS
authors.lastname: Miller
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley Berkeley, CA, USA.
authors.forename: Kyle R
authors.initials: KR
authors.lastname: Frischkorn
authors.affiliation: US Department of Energy Joint Genome Institute Walnut Creek, CA, USA.
authors.forename: Robin A
authors.initials: RA
authors.lastname: Ohm
authors.affiliation: Oak Ridge National LaboratoryOak Ridge, TN, USA; Graduate School of Genome Science and Technology, University of Tennessee-Oak Ridge National LaboratoryKnoxville, TN, USA.
authors.forename: Zhou
authors.initials: Z
authors.lastname: Li
authors.affiliation: US Department of Energy Joint Genome Institute Walnut Creek, CA, USA.
authors.forename: Kurt
authors.initials: K
authors.lastname: LaButti
authors.affiliation: US Department of Energy Joint Genome Institute Walnut Creek, CA, USA.
authors.forename: Alla
authors.initials: A
authors.lastname: Lapidus
authors.affiliation: US Department of Energy Joint Genome Institute Walnut Creek, CA, USA.
authors.forename: Anna
authors.initials: A
authors.lastname: Lipzen
authors.affiliation: US Department of Energy Joint Genome Institute Walnut Creek, CA, USA.
authors.forename: Cindy
authors.initials: C
authors.lastname: Chen
authors.affiliation: US Department of Energy Joint Genome Institute Walnut Creek, CA, USA.
authors.forename: Jenifer
authors.initials: J
authors.lastname: Johnson
authors.affiliation: US Department of Energy Joint Genome Institute Walnut Creek, CA, USA.
authors.forename: Erika A
authors.initials: EA
authors.lastname: Lindquist
authors.affiliation: Oak Ridge National Laboratory Oak Ridge, TN, USA.
authors.forename: Chongle
authors.initials: C
authors.lastname: Pan
authors.affiliation: Oak Ridge National Laboratory Oak Ridge, TN, USA.
authors.forename: Robert L
authors.initials: RL
authors.lastname: Hettich
authors.affiliation: US Department of Energy Joint Genome Institute Walnut Creek, CA, USA.
authors.forename: Igor V
authors.initials: IV
authors.lastname: Grigoriev
authors.affiliation: Earth Sciences Division, Lawrence Berkeley National Laboratory Berkeley, CA, USA.
authors.forename: Steven W
authors.initials: SW
authors.lastname: Singer
authors.affiliation: Department of Earth and Planetary Science, University of California, BerkeleyBerkeley, CA, USA; Department of Environmental Science, Policy, and Management, University of California, BerkeleyBerkeley, CA, USA.
authors.forename: Jillian F
authors.initials: JF
authors.lastname: Banfield
keywords: biofilm; carbon; fungi; metagenomics; nitrogen; proteomics; transcriptomics