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Title: Chronic Physical Disturbance Substantially Alters the Response of Biological Soil Crusts to a Wetting Pulse, as Characterized by Metatranscriptomic Sequencing

Abstract

Biological soil crusts (biocrusts) are microbial communities that are a feature of arid surface soils worldwide. In drylands where precipitation is pulsed and ephemeral, the ability of biocrust microbiota to rapidly initiate metabolic activity is critical to their survival. Community gene expression was compared after a short duration (1 h) wetting pulse in both intact and soils disturbed by chronic foot trampling. Across the metatranscriptomes the majority of transcripts were cyanobacterial in origin, suggesting that cyanobacteria accounted for the bulk of the transcriptionally active cells. Chronic trampling substantially altered the functional profile of the metatranscriptomes, specifically resulting in a significant decrease in transcripts for nitrogen fixation. Soil depth (biocrust and below crust) was a relatively small factor in differentiating the metatranscriptomes, suggesting that the metabolically active bacteria were similar between shallow soil horizons. The dry samples were consistently enriched for hydrogenase genes, indicating that molecular hydrogen may serve as an energy source for the desiccated soil communities. The water pulse was associated with a restructuring of the metatranscriptome, particularly for the biocrusts. Biocrusts increased transcripts for photosynthesis and carbon fixation, suggesting a rapid resuscitation upon wetting. In contrast, the trampled surface soils showed a much smaller response to wetting, indicatingmore » that trampling altered the metabolic response of the community. Finally, several biogeochemical cycling genes in carbon and nitrogen cycling were assessed for their change in abundance due to wetting in the biocrusts. Different transcripts encoding the same gene product did not show a consensus response, with some more abundant in dry or wet biocrusts, highlighting the challenges in relating transcript abundance to biogeochemical cycling rates. These observations demonstrate that metatranscriptome sequencing was able to distinguish alterations in the function of arid soil microbial communities at two varying temporal scales, a long-term ecosystems disturbance through foot trampling, and a short term wetting pulse. Thus, community metatranscriptomes have the potential to inform studies on the response and resilience of biocrusts to various environmental perturbations.« less

Authors:
 [1];  [2]; ORCiD logo [3]
  1. Connecticut Agricultural Experiment Station, New Haven, CT (United States). Dept. of Environmental Sciences
  2. Southwest Biological Science Center, Moab, UT (United States). United States Geological Survey, Moab
  3. 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 Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1479950
Report Number(s):
LA-UR-17-31418
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biological Science

Citation Formats

Steven, Blaire, Belnap, Jayne, and Kuske, Cheryl R. Chronic Physical Disturbance Substantially Alters the Response of Biological Soil Crusts to a Wetting Pulse, as Characterized by Metatranscriptomic Sequencing. United States: N. p., 2018. Web. doi:10.3389/fmicb.2018.02382.
Steven, Blaire, Belnap, Jayne, & Kuske, Cheryl R. Chronic Physical Disturbance Substantially Alters the Response of Biological Soil Crusts to a Wetting Pulse, as Characterized by Metatranscriptomic Sequencing. United States. https://doi.org/10.3389/fmicb.2018.02382
Steven, Blaire, Belnap, Jayne, and Kuske, Cheryl R. 2018. "Chronic Physical Disturbance Substantially Alters the Response of Biological Soil Crusts to a Wetting Pulse, as Characterized by Metatranscriptomic Sequencing". United States. https://doi.org/10.3389/fmicb.2018.02382. https://www.osti.gov/servlets/purl/1479950.
@article{osti_1479950,
title = {Chronic Physical Disturbance Substantially Alters the Response of Biological Soil Crusts to a Wetting Pulse, as Characterized by Metatranscriptomic Sequencing},
author = {Steven, Blaire and Belnap, Jayne and Kuske, Cheryl R.},
abstractNote = {Biological soil crusts (biocrusts) are microbial communities that are a feature of arid surface soils worldwide. In drylands where precipitation is pulsed and ephemeral, the ability of biocrust microbiota to rapidly initiate metabolic activity is critical to their survival. Community gene expression was compared after a short duration (1 h) wetting pulse in both intact and soils disturbed by chronic foot trampling. Across the metatranscriptomes the majority of transcripts were cyanobacterial in origin, suggesting that cyanobacteria accounted for the bulk of the transcriptionally active cells. Chronic trampling substantially altered the functional profile of the metatranscriptomes, specifically resulting in a significant decrease in transcripts for nitrogen fixation. Soil depth (biocrust and below crust) was a relatively small factor in differentiating the metatranscriptomes, suggesting that the metabolically active bacteria were similar between shallow soil horizons. The dry samples were consistently enriched for hydrogenase genes, indicating that molecular hydrogen may serve as an energy source for the desiccated soil communities. The water pulse was associated with a restructuring of the metatranscriptome, particularly for the biocrusts. Biocrusts increased transcripts for photosynthesis and carbon fixation, suggesting a rapid resuscitation upon wetting. In contrast, the trampled surface soils showed a much smaller response to wetting, indicating that trampling altered the metabolic response of the community. Finally, several biogeochemical cycling genes in carbon and nitrogen cycling were assessed for their change in abundance due to wetting in the biocrusts. Different transcripts encoding the same gene product did not show a consensus response, with some more abundant in dry or wet biocrusts, highlighting the challenges in relating transcript abundance to biogeochemical cycling rates. These observations demonstrate that metatranscriptome sequencing was able to distinguish alterations in the function of arid soil microbial communities at two varying temporal scales, a long-term ecosystems disturbance through foot trampling, and a short term wetting pulse. Thus, community metatranscriptomes have the potential to inform studies on the response and resilience of biocrusts to various environmental perturbations.},
doi = {10.3389/fmicb.2018.02382},
url = {https://www.osti.gov/biblio/1479950}, journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 9,
place = {United States},
year = {Mon Oct 08 00:00:00 EDT 2018},
month = {Mon Oct 08 00:00:00 EDT 2018}
}

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Cited by: 18 works
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Figures / Tables:

FIGURE 1 FIGURE 1: (A) Photograph of field plots. The control plots show well-developed biocrusts directly adjacent to a trampled plot (separated by a nylon rope). A pen is included for scale. (B) NMDS plot showing the relationship of metatranscriptome datasets. Intergroup distances were calculated with the Bray–Curtis metric. The colored ellipsesmore » are included as a visual aid only and were not part of the analysis. The groupings within each ellipse are indicated by the bolded text. The stress value of the ordination is indicated in the top left corner.« less

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Works referenced in this record:

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Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust
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Precipitation pulses and carbon fluxes in semiarid and arid ecosystems
journal, August 2004


Desiccation: An environmental and food industry stress that bacteria commonly face
journal, February 2018


Diversity in hydrogen evolution from bidirectional hydrogenases in cyanobacteria from terrestrial, freshwater and marine intertidal environments
journal, November 2012


Assembly, function and evolution of cyanobacterial carboxysomes
journal, June 2016


The role of the exopolysaccharides in enhancing hydraulic conductivity of biological soil crusts
journal, March 2012


Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils
journal, February 2014


Nitrogen status modulates the expression of RNA-binding proteins in cyanobacteria
journal, October 2003


Cyanobacteria track water in desert soils
journal, September 2001


Response and resilience of soil biocrust bacterial communities to chronic physical disturbance in arid shrublands
journal, November 2011


Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust
journal, June 2013


Near-optimal probabilistic RNA-seq quantification
journal, April 2016


Microbial colonization and controls in dryland systems
journal, July 2012


High-accuracy long-read amplicon sequences using unique molecular identifiers with Nanopore or PacBio sequencing
journal, January 2021


Changes in translational efficiency is a dominant regulatory mechanism in the environmental response of bacteria
journal, January 2013


Uptake hydrogenase in cyanobacteria: novel input from non-heterocystous strains
journal, February 2005


Growth rate-stoichiometry couplings in diverse biota
journal, October 2003


Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays
journal, July 2002


Relating the metatranscriptome and metagenome of the human gut
journal, May 2014


Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging
journal, August 2015


STAMP: statistical analysis of taxonomic and functional profiles
journal, July 2014


The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
journal, November 2013


In Planta Determination of the mRNA-Binding Proteome of Arabidopsis Etiolated Seedlings
journal, October 2016


Seed Germination and Dormancy.
journal, July 1997


Microenvironments and Microscale Productivity of Cyanobacterial Desert Crusts1
journal, October 1996


Precipitation pulses and soil CO 2 flux in a Sonoran Desert ecosystem
journal, February 2007


The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts
journal, October 1996


VEGAN, a package of R functions for community ecology
journal, April 2003


Interdependence of Cell Growth and Gene Expression: Origins and Consequences
journal, November 2010


De novo assembly and characterization of the transcriptome in the desiccation-tolerant moss Syntrichia caninervis
journal, January 2014


Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


IMP: a pipeline for reproducible reference-independent integrated metagenomic and metatranscriptomic analyses
journal, December 2016


Rapid Recovery of Cyanobacterial Pigments in Desiccated Biological Soil Crusts following Addition of Water
journal, November 2014


Soil bacterial and fungal community responses to nitrogen addition across soil depth and microhabitat in an arid shrubland
journal, September 2015


Determination of the Glycogen Content in Cyanobacteria
journal, July 2017


Works referencing / citing this record:

The Ecology of Subaerial Biofilms in Dry and Inhospitable Terrestrial Environments
journal, September 2019