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Title: Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil

Abstract

ABSTRACT Soil ecosystems harbor diverse microorganisms and yet remain only partially characterized as neither single-cell sequencing nor whole-community sequencing offers a complete picture of these complex communities. Thus, the genetic and metabolic potential of this “uncultivated majority” remains underexplored. To address these challenges, we applied a pooled-cell-sorting-based mini-metagenomics approach and compared the results to bulk metagenomics. Informatic binning of these data produced 200 mini-metagenome assembled genomes (sorted-MAGs) and 29 bulk metagenome assembled genomes (MAGs). The sorted and bulk MAGs increased the known phylogenetic diversity of soil taxa by 7.2% with respect to the Joint Genome Institute IMG/M database and showed clade-specific sequence recruitment patterns across diverse terrestrial soil metagenomes. Additionally, sorted-MAGs expanded the rare biosphere not captured through MAGs from bulk sequences, exemplified through phylogenetic and functional analyses of members of the phylum Bacteroidetes . Analysis of 67 Bacteroidetes sorted-MAGs showed conserved patterns of carbon metabolism across four clades. These results indicate that mini-metagenomics enables genome-resolved investigation of predicted metabolism and demonstrates the utility of combining metagenomics methods to tap into the diversity of heterogeneous microbial assemblages. IMPORTANCE Microbial ecologists have historically used cultivation-based approaches as well as amplicon sequencing and shotgun metagenomics to characterize microbial diversity in soil. However,more » challenges persist in the study of microbial diversity, including the recalcitrance of the majority of microorganisms to laboratory cultivation and limited sequence assembly from highly complex samples. The uncultivated majority thus remains a reservoir of untapped genetic diversity. To address some of the challenges associated with bulk metagenomics as well as low throughput of single-cell genomics, we applied flow cytometry-enabled mini-metagenomics to capture expanded microbial diversity from forest soil and compare it to soil bulk metagenomics. Our resulting data from this pooled-cell sorting approach combined with bulk metagenomics revealed increased phylogenetic diversity through novel soil taxa and rare biosphere members. In-depth analysis of genomes within the highly represented Bacteroidetes phylum provided insights into conserved and clade-specific patterns of carbon metabolism.« less

Authors:
; ORCiD logo; ; ; ; ; ; ORCiD logo; ; ; ORCiD logo; ; ORCiD logo;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA; National Institute of Food and Agriculture (NIFA); Austrian Science Fund (FWF); National Science Foundation (NSF)
OSTI Identifier:
1603713
Alternate Identifier(s):
OSTI ID: 1615320
Grant/Contract Number:  
AC02-05CH11231; 503125; P26392-B20; DEB 1237491; DEB 1456528
Resource Type:
Published Article
Journal Name:
mSystems
Additional Journal Information:
Journal Name: mSystems Journal Volume: 5 Journal Issue: 2; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Alteio, L. V., Schulz, F., Seshadri, R., Varghese, N., Rodriguez-Reillo, W., Ryan, E., Goudeau, D., Eichorst, S. A., Malmstrom, R. R., Bowers, R. M., Katz, L. A., Blanchard, J. L., Woyke, T., and Jansson, ed., Janet K.. Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil. United States: N. p., 2020. Web. doi:10.1128/mSystems.00768-19.
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Alteio, L. V., Schulz, F., Seshadri, R., Varghese, N., Rodriguez-Reillo, W., Ryan, E., Goudeau, D., Eichorst, S. A., Malmstrom, R. R., Bowers, R. M., Katz, L. A., Blanchard, J. L., Woyke, T., & Jansson, ed., Janet K.. Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil. United States. https://doi.org/10.1128/mSystems.00768-19
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Alteio, L. V., Schulz, F., Seshadri, R., Varghese, N., Rodriguez-Reillo, W., Ryan, E., Goudeau, D., Eichorst, S. A., Malmstrom, R. R., Bowers, R. M., Katz, L. A., Blanchard, J. L., Woyke, T., and Jansson, ed., Janet K.. Tue . "Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil". United States. https://doi.org/10.1128/mSystems.00768-19.
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@article{osti_1603713,
title = {Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil},
author = {Alteio, L. V. and Schulz, F. and Seshadri, R. and Varghese, N. and Rodriguez-Reillo, W. and Ryan, E. and Goudeau, D. and Eichorst, S. A. and Malmstrom, R. R. and Bowers, R. M. and Katz, L. A. and Blanchard, J. L. and Woyke, T. and Jansson, ed., Janet K.},
abstractNote = {ABSTRACT Soil ecosystems harbor diverse microorganisms and yet remain only partially characterized as neither single-cell sequencing nor whole-community sequencing offers a complete picture of these complex communities. Thus, the genetic and metabolic potential of this “uncultivated majority” remains underexplored. To address these challenges, we applied a pooled-cell-sorting-based mini-metagenomics approach and compared the results to bulk metagenomics. Informatic binning of these data produced 200 mini-metagenome assembled genomes (sorted-MAGs) and 29 bulk metagenome assembled genomes (MAGs). The sorted and bulk MAGs increased the known phylogenetic diversity of soil taxa by 7.2% with respect to the Joint Genome Institute IMG/M database and showed clade-specific sequence recruitment patterns across diverse terrestrial soil metagenomes. Additionally, sorted-MAGs expanded the rare biosphere not captured through MAGs from bulk sequences, exemplified through phylogenetic and functional analyses of members of the phylum Bacteroidetes . Analysis of 67 Bacteroidetes sorted-MAGs showed conserved patterns of carbon metabolism across four clades. These results indicate that mini-metagenomics enables genome-resolved investigation of predicted metabolism and demonstrates the utility of combining metagenomics methods to tap into the diversity of heterogeneous microbial assemblages. IMPORTANCE Microbial ecologists have historically used cultivation-based approaches as well as amplicon sequencing and shotgun metagenomics to characterize microbial diversity in soil. However, challenges persist in the study of microbial diversity, including the recalcitrance of the majority of microorganisms to laboratory cultivation and limited sequence assembly from highly complex samples. The uncultivated majority thus remains a reservoir of untapped genetic diversity. To address some of the challenges associated with bulk metagenomics as well as low throughput of single-cell genomics, we applied flow cytometry-enabled mini-metagenomics to capture expanded microbial diversity from forest soil and compare it to soil bulk metagenomics. Our resulting data from this pooled-cell sorting approach combined with bulk metagenomics revealed increased phylogenetic diversity through novel soil taxa and rare biosphere members. In-depth analysis of genomes within the highly represented Bacteroidetes phylum provided insights into conserved and clade-specific patterns of carbon metabolism.},
doi = {10.1128/mSystems.00768-19},
journal = {mSystems},
number = 2,
volume = 5,
place = {United States},
year = {2020},
month = {3}
}
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https://doi.org/10.1128/mSystems.00768-19
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Figures / Tables:

FIG 1 FIG 1: Overview of mini-metagenome and bulk metagenome approaches used in this study. (A) Mini-metagenomics performed on four soil samples, including one heated sample from the top organic soil, one heated sample from the lower mineral soil, one control organic sample, and one control mineral sample (n = 4). Cellsmore » were separated from soil particles using a mild detergent, followed by vortex mixing, centrifugation, and filtration through a 5- μm-pore-size syringe filter. Suspended cells were stained with SYBR green and sorted into 90 pools of 100 cells each, generating 359 mini-metagenomes. (B) Bulk metagenomic sequencing conducted on the four soils that were used in mini-metagenomics. (C) Following nucleic acid extraction, libraries were prepared, and shotgun sequencing was performed. Sequence data underwent assembly and quality control. Data were binned and assessed for bin quality. Only medium-quality genome bins with estimates of 50% completeness, 10% contamination, and 10% strain heterogeneity were used in downstream phylogenomic and functional analyses. Further details are provided in Materials and Methods.« less
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