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Title: Isolation of a significant fraction of non-phototroph diversity from a desert Biological Soil Crust

Abstract

Biological Soil Crusts (BSCs) are organosedimentary assemblages comprised of microbes and minerals in topsoil of terrestrial environments. BSCs strongly impact soil quality in dryland ecosystems (e.g., soil structure and nutrient yields) due to pioneer species such as Microcoleus vaginatus; phototrophs that produce filaments that bind the soil together, and support an array of heterotrophic microorganisms. These microorganisms in turn contribute to soil stability and biogeochemistry of BSCs. Non cyanobacterial populations of BSCs are less well known than cyanobacterial populations. Therefore, we attempted to isolate a broad range of numerically significant and phylogenetically representative BSC aerobic heterotrophs. Combining simple pre treatments (hydration of BSCs under dark and light) and isolation strategies (media with varying nutrient availability and protection from oxidative stress) we recovered 402 bacterial and one fungal isolate in axenic culture, which comprised 116 phylotypes (at 97% 16S rRNA gene sequence homology), 115 bacterial and one fungal. Each medium enriched a mostly distinct subset of phylotypes, and cultivated phylotypes varied due to the BSC pre-treatment. The fraction of the total phylotype diversity isolated, weighted by relative abundance in the community, was determined by the overlap between isolate sequences and OTUs reconstructed from metagenome or metatranscriptome reads. Together, more than 8%more » of relative abundance of OTUs in the metagenome was represented by our isolates, a cultivation efficiency much larger than typically expected from most soils. We conclude that simple cultivation procedures combined with specific pre-treatment of samples afford a significant reduction in the culturability gap, enabling physiological and metabolic assays that rely on ecologically relevant axenic cultures.« less

Authors:
 [1];  [2];  [3];  [3];  [3];  [2];  [2];  [2];  [3];  [4];  [3];  [3];  [5]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Quantitative Microbial Ecology Group, Amsterdam (Netherlands)
  2. Arizona State Univ., Tucson, AZ (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Arizona State Univ., Tucson, AZ (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1200858
Alternate Identifier(s):
OSTI ID: 1407291
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; biological soil crusts; culturability; isolation; dryland microbiology; microbial diversity

Citation Formats

Nunes da Rocha, Ulisses, Cadillo-Quiroz, Hinsby, Karaoz, Ulas, Rajeev, Lara, Klitgord, Niels, Dunn, Sean, Truong, Viet, Buenrostro, Mayra, Bowen, Benjamin P., Garcia-Pichel, Ferran, Mukhopadhyay, Aindrila, Northen, Trent R., and Brodie, Eoin L. Isolation of a significant fraction of non-phototroph diversity from a desert Biological Soil Crust. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.00277.
Nunes da Rocha, Ulisses, Cadillo-Quiroz, Hinsby, Karaoz, Ulas, Rajeev, Lara, Klitgord, Niels, Dunn, Sean, Truong, Viet, Buenrostro, Mayra, Bowen, Benjamin P., Garcia-Pichel, Ferran, Mukhopadhyay, Aindrila, Northen, Trent R., & Brodie, Eoin L. Isolation of a significant fraction of non-phototroph diversity from a desert Biological Soil Crust. United States. https://doi.org/10.3389/fmicb.2015.00277
Nunes da Rocha, Ulisses, Cadillo-Quiroz, Hinsby, Karaoz, Ulas, Rajeev, Lara, Klitgord, Niels, Dunn, Sean, Truong, Viet, Buenrostro, Mayra, Bowen, Benjamin P., Garcia-Pichel, Ferran, Mukhopadhyay, Aindrila, Northen, Trent R., and Brodie, Eoin L. Tue . "Isolation of a significant fraction of non-phototroph diversity from a desert Biological Soil Crust". United States. https://doi.org/10.3389/fmicb.2015.00277. https://www.osti.gov/servlets/purl/1200858.
@article{osti_1200858,
title = {Isolation of a significant fraction of non-phototroph diversity from a desert Biological Soil Crust},
author = {Nunes da Rocha, Ulisses and Cadillo-Quiroz, Hinsby and Karaoz, Ulas and Rajeev, Lara and Klitgord, Niels and Dunn, Sean and Truong, Viet and Buenrostro, Mayra and Bowen, Benjamin P. and Garcia-Pichel, Ferran and Mukhopadhyay, Aindrila and Northen, Trent R. and Brodie, Eoin L.},
abstractNote = {Biological Soil Crusts (BSCs) are organosedimentary assemblages comprised of microbes and minerals in topsoil of terrestrial environments. BSCs strongly impact soil quality in dryland ecosystems (e.g., soil structure and nutrient yields) due to pioneer species such as Microcoleus vaginatus; phototrophs that produce filaments that bind the soil together, and support an array of heterotrophic microorganisms. These microorganisms in turn contribute to soil stability and biogeochemistry of BSCs. Non cyanobacterial populations of BSCs are less well known than cyanobacterial populations. Therefore, we attempted to isolate a broad range of numerically significant and phylogenetically representative BSC aerobic heterotrophs. Combining simple pre treatments (hydration of BSCs under dark and light) and isolation strategies (media with varying nutrient availability and protection from oxidative stress) we recovered 402 bacterial and one fungal isolate in axenic culture, which comprised 116 phylotypes (at 97% 16S rRNA gene sequence homology), 115 bacterial and one fungal. Each medium enriched a mostly distinct subset of phylotypes, and cultivated phylotypes varied due to the BSC pre-treatment. The fraction of the total phylotype diversity isolated, weighted by relative abundance in the community, was determined by the overlap between isolate sequences and OTUs reconstructed from metagenome or metatranscriptome reads. Together, more than 8% of relative abundance of OTUs in the metagenome was represented by our isolates, a cultivation efficiency much larger than typically expected from most soils. We conclude that simple cultivation procedures combined with specific pre-treatment of samples afford a significant reduction in the culturability gap, enabling physiological and metabolic assays that rely on ecologically relevant axenic cultures.},
doi = {10.3389/fmicb.2015.00277},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Tue Apr 14 00:00:00 EDT 2015},
month = {Tue Apr 14 00:00:00 EDT 2015}
}

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Works referenced in this record:

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journal, October 2009


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journal, May 2010


Diversity of free-living and lichenized fungal communities in biological soil crusts of the Sultanate of Oman and their role in improving soil properties
journal, February 2013


Response and resilience of soil biocrust bacterial communities to chronic physical disturbance in arid shrublands
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Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust
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Search and clustering orders of magnitude faster than BLAST
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UCHIME improves sensitivity and speed of chimera detection
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SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes
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Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy
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Duplex-specific nuclease efficiently removes rRNA for prokaryotic RNA-seq
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Dyadobacter crusticola sp. nov., from biological soil crusts in the Colorado Plateau, USA, and an emended description of the genus Dyadobacter Chelius and Triplett 2000
journal, May 2005

  • Reddy, G. S. N.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 3
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Sphingomonas mucosissima sp. nov. and Sphingomonas desiccabilis sp. nov., from biological soil crusts in the Colorado Plateau, USA
journal, May 2007

  • Reddy, G. S. N.; Garcia-Pichel, F.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 5
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Exophiala crusticola anam. nov. (affinity Herpotrichiellaceae), a novel black yeast from biological soil crusts in the Western United States
journal, November 2006

  • Bates, S. T.; Reddy, G. S. N.; Garcia-Pichel, F.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 11
  • DOI: 10.1099/ijs.0.64332-0

Modestobacter versicolor sp. nov., an actinobacterium from biological soil crusts that produces melanins under oligotrophy, with emended descriptions of the genus Modestobacter and Modestobacter multiseptatus Mevs et al. 2000
journal, September 2007

  • Reddy, G. S. N.; Potrafka, R. M.; Garcia-Pichel, F.
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The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts
journal, October 1996


Combination of high throughput cultivation and dsr A sequencing for assessment of sulfate-reducing bacteria diversity in sediments
journal, August 2012


Targeted and shotgun metagenomic approaches provide different descriptions of dryland soil microbial communities in a manipulated field study: Sequencing to describe dryland soil communities
journal, February 2012


Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior
journal, January 2006


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Are Uncultivated Bacteria Really Uncultivable?
journal, January 2012

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FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
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Photosynthesis and Water Relations of Lichen Soil Crusts: Field Measurements in the Coastal Fog Zone of the Namib Desert
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Works referencing / citing this record:

Biocrust morphology is linked to marked differences in microbial community composition
journal, October 2017

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Exometabolite niche partitioning among sympatric soil bacteria
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Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018


Distinct interacting core taxa in co-occurrence networks enable discrimination of polymicrobial oral diseases with similar symptoms
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Optimizing the Production of Nursery-Based Biological Soil Crusts for Restoration of Arid Land Soils
journal, May 2019

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Status of the Archaeal and Bacterial Census: an Update
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A “Cultural” Renaissance: Genomics Breathes New Life into an Old Craft
journal, May 2019


The Compositionally Distinct Cyanobacterial Biocrusts From Brazilian Savanna and Their Environmental Drivers of Community Diversity
journal, December 2019

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


Exometabolite niche partitioning among sympatric soil bacteria
journal, September 2015

  • Baran, Richard; Brodie, Eoin L.; Mayberry-Lewis, Jazmine
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms9289

Distinct interacting core taxa in co-occurrence networks enable discrimination of polymicrobial oral diseases with similar symptoms
journal, August 2016

  • Shiba, Takahiko; Watanabe, Takayasu; Kachi, Hirokazu
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep30997

Optimizing the Production of Nursery-Based Biological Soil Crusts for Restoration of Arid Land Soils
journal, May 2019

  • Bethany, Julie; Giraldo-Silva, Ana; Nelson, Corey
  • Applied and Environmental Microbiology, Vol. 85, Issue 15
  • DOI: 10.1128/aem.00735-19

After All, Only Millions?
journal, July 2016


A “Cultural” Renaissance: Genomics Breathes New Life into an Old Craft
journal, May 2019


The Cacti Microbiome: Interplay between Habitat-Filtering and Host-Specificity
journal, February 2016

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Bioweathering Potential of Cultivable Fungi Associated with Semi-Arid Surface Microhabitats of Mayan Buildings
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The Compositionally Distinct Cyanobacterial Biocrusts From Brazilian Savanna and Their Environmental Drivers of Community Diversity
journal, December 2019

  • Machado-de-Lima, Náthali Maria; Fernandes, Vanessa Moreira Câmara; Roush, Daniel
  • Frontiers in Microbiology, Vol. 10
  • DOI: 10.3389/fmicb.2019.02798