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

Renmao Tian; Daliang Ning; Zhili He; Ping Zhang; Sarah J Spencer; Shuhong Gao; Weiling Shi; Linwei Wu; Ya Zhang; Yunfeng Yang; Benjamin G Adams; Andrea M Rocha; Brittny L Detienne; Kenneth A Lowe; Dominique C Joyner; Dawn M Klingeman; Adam P Arkin; Matthew W Fields; Terry C Hazen; David A Stahl; Eric J Alm; Jizhong Zhou

doi:10.1186/s40168-020-00825-w

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

Microbiome. 2020 Apr 6;8(1):51. doi: 10.1186/s40168-020-00825-w.

Authors

Renmao Tian¹, Daliang Ning¹, Zhili He¹, Ping Zhang¹, Sarah J Spencer², Shuhong Gao¹, Weiling Shi¹, Linwei Wu¹, Ya Zhang¹, Yunfeng Yang³, Benjamin G Adams⁴, Andrea M Rocha⁵, Brittny L Detienne⁴, Kenneth A Lowe⁵, Dominique C Joyner⁴, Dawn M Klingeman⁵, Adam P Arkin^{6

7}, Matthew W Fields⁸, Terry C Hazen^{4

5}, David A Stahl⁹, Eric J Alm², Jizhong Zhou^{10

11

12}

Affiliations

¹ Department of Microbiology and Plant Biology, Institute for Environmental Genomics, University of Oklahoma, Norman, OK, USA.
² Biological Engineering Department, Massachusetts Institute of Technology, Cambridge, MA, USA.
³ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China.
⁴ Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, TN, USA.
⁵ Oak Ridge National Laboratory, Biosciences Division, Oak Ridge, TN, USA.
⁶ Department of Bioengineering, University of California, Berkeley, CA, USA.
⁷ Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
⁸ Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA.
⁹ Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, USA.
¹⁰ Department of Microbiology and Plant Biology, Institute for Environmental Genomics, University of Oklahoma, Norman, OK, USA. jzhou@ou.edu.
¹¹ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China. jzhou@ou.edu.
¹² Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA. jzhou@ou.edu.

Abstract

Background: 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.

Results: Here, 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 features and the groundwater environmental conditions, our results provide important insights into the functions and evolution of this CPR group.

Conclusions: We found that Patescibacteria has streamlined many functions while acquiring advantages such as avoiding phage invasion, to adapt to the groundwater environment. The unique features of small genome size, ultra-small cell size, and lacking CRISPR of this large lineage are bringing new understandings on life of Bacteria. Our results provide important insights into the mechanisms for adaptation of the superphylum in the groundwater environments, and demonstrate a case where less is more, and small is mighty.

Keywords: Candidate phylum radiation; Genome reduction; Groundwater; Superphylum Patescibacteria.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Adaptation, Physiological*
Bacteria / genetics*
Fermentation
Genome Size*
Genome, Bacterial*
Groundwater / microbiology*
Metabolic Networks and Pathways
Metagenomics