Title: Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity

Abstract

The newly defined superphylum Patescibacteria such as Parcubacteria (OD1) and Microgenomates (OP11) has been found to be prevalent in groundwater, sediment, lake, and other aquifer environments. Recently increasing attention has been paid to this diverse superphylum including > 20 candidate phyla (a large part of the candidate phylum radiation, CPR) because it refreshed our view of the tree of life. However, adaptive traits contributing to its prevalence are still not well known.ResultsHere, we investigated the genomic features and metabolic pathways of Patescibacteria in groundwater through genome-resolved metagenomics analysis of >600 Gbp sequence data. We observed that, while the members of Patescibacteria have reduced genomes (~ 1 Mbp) exclusively, functions essential to growth and reproduction such as genetic information processing were retained. Surprisingly, they have sharply reduced redundant and nonessential functions, including specific metabolic activities and stress response systems. The Patescibacteria have ultra-small cells and simplified membrane structures, including flagellar assembly, transporters, and two-component systems. Despite the lack of CRISPR viral defense, the bacteria may evade predation through deletion of common membrane phage receptors and other alternative strategies, which may explain the low representation of prophage proteins in their genomes and lack of CRISPR. By establishing the linkages between bacterial featuresmore » and the groundwater environmental conditions, our results provide important insights into the functions and evolution of this CPR group.« less

Authors:

Tian, Renmao ^[1]; Ning, Daliang ^[1]; He, Zhili ^[1]; Zhang, Ping ^[1]; Spencer, Sarah J. ^[2]; Gao, Shuhong ^[1]; Shi, Weiling ^[1]; Wu, Linwei ^[1]; Zhang, Ya ^[1]; Yang, Yunfeng ^[3]; Adams, Benjamin G. ^[4]; Rocha, Andrea M. ^[5]; Detienne, Brittny L. ^[4]; Lowe, Kenneth A. ^[5]; Joyner, Dominique C. ^[4]; Klingeman, Dawn M.  ^[5];

• Search DOE PAGES for author "Klingeman, Dawn M."
• Search DOE PAGES for ORCID "0000-0002-4307-2560"

Arkin, Adam P. ^[6]; Fields, Matthew W. ^[7]; Hazen, Terry C.  ^[8];

• Search DOE PAGES for author "Hazen, Terry C."
• Search DOE PAGES for ORCID "0000-0002-2536-9993"

Stahl, David A. ^[9] more »; Alm, Eric J. ^[2]; Zhou, Jizhong ^[10] « less

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+ Show Author Affiliations

1. Univ. of Oklahoma, Norman, OK (United States)
2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
3. Tsinghua Univ., Beijing (China)
4. Univ. of Tennessee, Knoxville, TN (United States)
5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
6. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
7. Montana State Univ., Bozeman, MT (United States)
8. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
9. Univ. of Washington, Seattle, WA (United States)
10. Univ. of Oklahoma, Norman, OK (United States); Tsinghua Univ., Beijing (China); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Publication Date:

Mon Apr 06 00:00:00 EDT 2020

Research Org.:

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

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:

1651273

Alternate Identifier(s):

OSTI ID: 1631654

Grant/Contract Number:  

AC05-00OR22725; AC02-05CH11231

Resource Type:

Accepted Manuscript

Journal Name:

Microbiome

Additional Journal Information:

Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2049-2618

Publisher:

BioMed Central

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; Superphylum Patescibacteria; Candidate phylum radiation; Groundwater; Genome reduction