Genomic insights into diverse bacterial taxa that degrade extracellular DNA in marine sediments

Kenneth Wasmund; Claus Pelikan; Arno Schintlmeister; Michael Wagner; Margarete Watzka; Andreas Richter; Srijak Bhatnagar; Amy Noel; Casey R.J. Hubert; Thomas Rattei; Thilo Hofmann; Bela Hausmann; Craig W. Herbold; Alexander Loy

doi:10.1038/s41564-021-00917-9

Genomic insights into diverse bacterial taxa that degrade extracellular DNA in marine sediments

Kenneth Wasmund^*, Claus Pelikan, Arno Schintlmeister, Michael Wagner, Margarete Watzka, Andreas Richter, Srijak Bhatnagar, Amy Noel, Casey R.J. Hubert, Thomas Rattei, Thilo Hofmann, Bela Hausmann, Craig W. Herbold, Alexander Loy

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › Research › peer-review

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Abstract

Extracellular DNA is a major macromolecule in global element cycles, and is a particularly crucial phosphorus, nitrogen and carbon source for microorganisms in the seafloor. Nevertheless, the identities, ecophysiology and genetic features of DNA-foraging microorganisms in marine sediments are largely unknown. Here, we combined microcosm experiments, DNA stable isotope probing (SIP), single-cell SIP using nano-scale secondary isotope mass spectrometry (NanoSIMS) and genome-centric metagenomics to study microbial catabolism of DNA and its subcomponents in marine sediments. ¹³C-DNA added to sediment microcosms was largely degraded within 10 d and mineralized to ¹³CO₂. SIP probing of DNA revealed diverse ‘Candidatus Izemoplasma’, Lutibacter, Shewanella and Fusibacteraceae incorporated DNA-derived ¹³C-carbon. NanoSIMS confirmed incorporation of ¹³C into individual bacterial cells of Fusibacteraceae sorted from microcosms. Genomes of the ¹³C-labelled taxa all encoded enzymatic repertoires for catabolism of DNA or subcomponents of DNA. Comparative genomics indicated that diverse ‘Candidatus Izemoplasmatales’ (former Tenericutes) are exceptional because they encode multiple (up to five) predicted extracellular nucleases and are probably specialized DNA-degraders. Analyses of additional sediment metagenomes revealed extracellular nuclease genes are prevalent among Bacteroidota at diverse sites. Together, our results reveal the identities and functional properties of microorganisms that may contribute to the key ecosystem function of degrading and recycling DNA in the seabed.

Original language	English
Journal	Nature Microbiology
Volume	6
Issue number	7
Pages (from-to)	885-898
Number of pages	14
ISSN	2058-5276
DOIs	https://doi.org/10.1038/s41564-021-00917-9
Publication status	Published - Jul 2021

Bibliographical note

This Article was originally published with an incorrect copyright status, and should have been Open Access. This error has now been corrected and the Article is now published under a Creative Commons licence CC BY 4.0.

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© 2021, The Author(s), under exclusive licence to Springer Nature Limited.

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s41564-021-00917-9Final published version, 12 MBLicence: CC BY 4.0

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Wasmund, K., Pelikan, C., Schintlmeister, A., Wagner, M., Watzka, M., Richter, A., Bhatnagar, S., Noel, A., Hubert, C. R. J., Rattei, T., Hofmann, T., Hausmann, B., Herbold, C. W., & Loy, A. (2021). Genomic insights into diverse bacterial taxa that degrade extracellular DNA in marine sediments. Nature Microbiology, 6(7), 885-898. https://doi.org/10.1038/s41564-021-00917-9

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title = "Genomic insights into diverse bacterial taxa that degrade extracellular DNA in marine sediments",

abstract = "Extracellular DNA is a major macromolecule in global element cycles, and is a particularly crucial phosphorus, nitrogen and carbon source for microorganisms in the seafloor. Nevertheless, the identities, ecophysiology and genetic features of DNA-foraging microorganisms in marine sediments are largely unknown. Here, we combined microcosm experiments, DNA stable isotope probing (SIP), single-cell SIP using nano-scale secondary isotope mass spectrometry (NanoSIMS) and genome-centric metagenomics to study microbial catabolism of DNA and its subcomponents in marine sediments. 13C-DNA added to sediment microcosms was largely degraded within 10 d and mineralized to 13CO2. SIP probing of DNA revealed diverse {\textquoteleft}Candidatus Izemoplasma{\textquoteright}, Lutibacter, Shewanella and Fusibacteraceae incorporated DNA-derived 13C-carbon. NanoSIMS confirmed incorporation of 13C into individual bacterial cells of Fusibacteraceae sorted from microcosms. Genomes of the 13C-labelled taxa all encoded enzymatic repertoires for catabolism of DNA or subcomponents of DNA. Comparative genomics indicated that diverse {\textquoteleft}Candidatus Izemoplasmatales{\textquoteright} (former Tenericutes) are exceptional because they encode multiple (up to five) predicted extracellular nucleases and are probably specialized DNA-degraders. Analyses of additional sediment metagenomes revealed extracellular nuclease genes are prevalent among Bacteroidota at diverse sites. Together, our results reveal the identities and functional properties of microorganisms that may contribute to the key ecosystem function of degrading and recycling DNA in the seabed.",

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note = "This Article was originally published with an incorrect copyright status, and should have been Open Access. This error has now been corrected and the Article is now published under a Creative Commons licence CC BY 4.0. Publisher Copyright: {\textcopyright} 2021, The Author(s), under exclusive licence to Springer Nature Limited.",

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AU - Bhatnagar, Srijak

AU - Noel, Amy

AU - Hubert, Casey R.J.

AU - Rattei, Thomas

AU - Hofmann, Thilo

AU - Hausmann, Bela

AU - Herbold, Craig W.

AU - Loy, Alexander

N1 - This Article was originally published with an incorrect copyright status, and should have been Open Access. This error has now been corrected and the Article is now published under a Creative Commons licence CC BY 4.0. Publisher Copyright: © 2021, The Author(s), under exclusive licence to Springer Nature Limited.

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Y1 - 2021/7

N2 - Extracellular DNA is a major macromolecule in global element cycles, and is a particularly crucial phosphorus, nitrogen and carbon source for microorganisms in the seafloor. Nevertheless, the identities, ecophysiology and genetic features of DNA-foraging microorganisms in marine sediments are largely unknown. Here, we combined microcosm experiments, DNA stable isotope probing (SIP), single-cell SIP using nano-scale secondary isotope mass spectrometry (NanoSIMS) and genome-centric metagenomics to study microbial catabolism of DNA and its subcomponents in marine sediments. 13C-DNA added to sediment microcosms was largely degraded within 10 d and mineralized to 13CO2. SIP probing of DNA revealed diverse ‘Candidatus Izemoplasma’, Lutibacter, Shewanella and Fusibacteraceae incorporated DNA-derived 13C-carbon. NanoSIMS confirmed incorporation of 13C into individual bacterial cells of Fusibacteraceae sorted from microcosms. Genomes of the 13C-labelled taxa all encoded enzymatic repertoires for catabolism of DNA or subcomponents of DNA. Comparative genomics indicated that diverse ‘Candidatus Izemoplasmatales’ (former Tenericutes) are exceptional because they encode multiple (up to five) predicted extracellular nucleases and are probably specialized DNA-degraders. Analyses of additional sediment metagenomes revealed extracellular nuclease genes are prevalent among Bacteroidota at diverse sites. Together, our results reveal the identities and functional properties of microorganisms that may contribute to the key ecosystem function of degrading and recycling DNA in the seabed.

AB - Extracellular DNA is a major macromolecule in global element cycles, and is a particularly crucial phosphorus, nitrogen and carbon source for microorganisms in the seafloor. Nevertheless, the identities, ecophysiology and genetic features of DNA-foraging microorganisms in marine sediments are largely unknown. Here, we combined microcosm experiments, DNA stable isotope probing (SIP), single-cell SIP using nano-scale secondary isotope mass spectrometry (NanoSIMS) and genome-centric metagenomics to study microbial catabolism of DNA and its subcomponents in marine sediments. 13C-DNA added to sediment microcosms was largely degraded within 10 d and mineralized to 13CO2. SIP probing of DNA revealed diverse ‘Candidatus Izemoplasma’, Lutibacter, Shewanella and Fusibacteraceae incorporated DNA-derived 13C-carbon. NanoSIMS confirmed incorporation of 13C into individual bacterial cells of Fusibacteraceae sorted from microcosms. Genomes of the 13C-labelled taxa all encoded enzymatic repertoires for catabolism of DNA or subcomponents of DNA. Comparative genomics indicated that diverse ‘Candidatus Izemoplasmatales’ (former Tenericutes) are exceptional because they encode multiple (up to five) predicted extracellular nucleases and are probably specialized DNA-degraders. Analyses of additional sediment metagenomes revealed extracellular nuclease genes are prevalent among Bacteroidota at diverse sites. Together, our results reveal the identities and functional properties of microorganisms that may contribute to the key ecosystem function of degrading and recycling DNA in the seabed.

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ER -

Genomic insights into diverse bacterial taxa that degrade extracellular DNA in marine sediments

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