Genomic and environmental controls on Castellaniella biogeography in an anthropogenically disturbed subsurface

Jennifer L Goff; Elizabeth G Szink; Konnor L Durrence; Lauren M Lui; Torben N Nielsen; Jennifer V Kuehl; Kristopher A Hunt; John-Marc Chandonia; Jiawen Huang; Michael P Thorgersen; Farris L Poole 2nd; David A Stahl; Romy Chakraborty; Adam M Deutschbauer; Adam P Arkin; Michael W W Adams

doi:10.1186/s40793-024-00570-9

Genomic and environmental controls on Castellaniella biogeography in an anthropogenically disturbed subsurface

Environ Microbiome. 2024 Apr 26;19(1):26. doi: 10.1186/s40793-024-00570-9.

Authors

Jennifer L Goff^#^{1

2}, Elizabeth G Szink^#¹, Konnor L Durrence¹, Lauren M Lui³, Torben N Nielsen³, Jennifer V Kuehl³, Kristopher A Hunt⁴, John-Marc Chandonia³, Jiawen Huang⁵, Michael P Thorgersen¹, Farris L Poole 2nd¹, David A Stahl⁴, Romy Chakraborty⁵, Adam M Deutschbauer³, Adam P Arkin^{3

6}, Michael W W Adams⁷

Affiliations

¹ Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA.
² State University of New York College of Environmental Science and Forestry, Syracuse, NY, USA.
³ Environmental Genomics and Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
⁴ Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, USA.
⁵ Earth and Environmental Science Area, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
⁶ Department of Bioengineering, University of California-Berkeley, Berkeley, CA, USA.
⁷ Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA. adamsm@uga.edu.

^# Contributed equally.

Abstract

Castellaniella species have been isolated from a variety of mixed-waste environments including the nitrate and multiple metal-contaminated subsurface at the Oak Ridge Reservation (ORR). Previous studies examining microbial community composition and nitrate removal at ORR during biostimulation efforts reported increased abundances of members of the Castellaniella genus concurrent with increased denitrification rates. Thus, we asked how genomic and abiotic factors control the Castellaniella biogeography at the site to understand how these factors may influence nitrate transformation in an anthropogenically impacted setting. We report the isolation and characterization of several Castellaniella strains from the ORR subsurface. Five of these isolates match at 100% identity (at the 16S rRNA gene V4 region) to two Castellaniella amplicon sequence variants (ASVs), ASV1 and ASV2, that have persisted in the ORR subsurface for at least 2 decades. However, ASV2 has consistently higher relative abundance in samples taken from the site and was also the dominant blooming denitrifier population during a prior biostimulation effort. We found that the ASV2 representative strain has greater resistance to mixed metal stress than the ASV1 representative strains. We attribute this resistance, in part, to the large number of unique heavy metal resistance genes identified on a genomic island in the ASV2 representative genome. Additionally, we suggest that the relatively lower fitness of ASV1 may be connected to the loss of the nitrous oxide reductase (nos) operon (and associated nitrous oxide reductase activity) due to the insertion at this genomic locus of a mobile genetic element carrying copper resistance genes. This study demonstrates the value of integrating genomic, environmental, and phenotypic data to characterize the biogeography of key microorganisms in contaminated sites.

Keywords: Acid tolerance; Contamination; Heavy metals; Mobile genetic elements; Nitrate; Pangenome.

Abstract

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