Continuous cultivation of the lithoautotrophic nitrate‐reducing Fe( II )‐oxidizing culture KS in a chemostat bioreactor

Timm Bayer; Elizabeth J. Tomaszewski; Casey Bryce; Andreas Kappler; James M. Byrne

doi:10.1111/1758-2229.13149

Continuous cultivation of the lithoautotrophic nitrate‐reducing Fe( II )‐oxidizing culture KS in a chemostat bioreactor

Timm Bayer, Elizabeth J. Tomaszewski, Casey Bryce, Andreas Kappler, James M. Byrne^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

Abstract

Laboratory-based studies on microbial Fe(II) oxidation are commonly performed for 5–10 days in small volumes with high substrate concentrations, resulting in geochemical gradients and volumetric effects caused by sampling. We used a chemostat to enable uninterrupted supply of medium and investigated autotrophic nitrate-reducing Fe(II)-oxidizing culture KS for 24 days. We analysed Fe- and N-speciation, cell-mineral associations, and the identity of minerals. Results were compared to batch systems (50 and 700 mL—static/shaken). The Fe(II) oxidation rate was highest in the chemostat with 7.57 mM Fe(II) d−1, while the extent of oxidation was similar to the other experimental setups (average oxidation of 92% of all Fe(II)). Short-range ordered Fe(III) phases, presumably ferrihydrite, precipitated and later goethite was detected in the chemostat. The 1 mM solid phase Fe(II) remained in the chemostat, up to 15 μM of reactive nitrite was measured, and 42% of visualized cells were partially or completely mineral-encrusted, likely caused by abiotic oxidation of Fe(II) by nitrite. Despite (partial) encrustation, cells were still viable. Our results show that even with similar oxidation rates as in batch cultures, cultivating Fe(II)-oxidizing microorganisms under continuous conditions reveals the importance of reactive nitrogen intermediates on Fe(II) oxidation, mineral formation and cell–mineral interactions.

Original language	English
Pages (from-to)	324-334
Number of pages	11
Journal	Environmental Microbiology Reports
Volume	15
Issue number	4
Early online date	29 Mar 2023
DOIs	https://doi.org/10.1111/1758-2229.13149
Publication status	E-pub ahead of print - 29 Mar 2023

Bibliographical note

Funding Information:
The authors thank Natalia Jakus for μ-XRD measurements and help with sample analysis. Markus Turad and Ronny Löffler (LISA+, University of Tübingen) for access to and help with scanning electron microscopy as well as Hartmut Schulz for help with scanning electron microscopy. Julian Sorwat and Manuel Schad for Mössbauer measurements. Lars Grimm for help with cultivation of culture KS. The authors acknowledge APS for XAS measurements: MRCAT operations are supported by the Department of Energy and the MRCAT member institutions. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. The authors acknowledge funding from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; BY 82/2-1) awarded to J. M. Byrne as well as infrastructural support by the DFG under Germany's Excellence Strategy, cluster of Excellence EXC2124, project ID 390838134. The authors also thank UK Research and Innovation for providing the grant: MR/V023918/1.

Funding Information:
The authors thank Natalia Jakus for μ‐XRD measurements and help with sample analysis. Markus Turad and Ronny Löffler (LISA, University of Tübingen) for access to and help with scanning electron microscopy as well as Hartmut Schulz for help with scanning electron microscopy. Julian Sorwat and Manuel Schad for Mössbauer measurements. Lars Grimm for help with cultivation of culture KS. The authors acknowledge APS for XAS measurements: MRCAT operations are supported by the Department of Energy and the MRCAT member institutions. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE‐AC02‐06CH11357. The authors acknowledge funding from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; BY 82/2‐1) awarded to J. M. Byrne as well as infrastructural support by the DFG under Germany's Excellence Strategy, cluster of Excellence EXC2124, project ID 390838134. The authors also thank UK Research and Innovation for providing the grant: MR/V023918/1. +

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© 2023 The Authors. Environmental Microbiology Reports published by Applied Microbiology International and John Wiley & Sons Ltd.

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@article{48e80ed980cc4a6aaf17124f91fa3bf2,

title = "Continuous cultivation of the lithoautotrophic nitrate‐reducing Fe( II )‐oxidizing culture KS in a chemostat bioreactor",

abstract = "Laboratory-based studies on microbial Fe(II) oxidation are commonly performed for 5–10 days in small volumes with high substrate concentrations, resulting in geochemical gradients and volumetric effects caused by sampling. We used a chemostat to enable uninterrupted supply of medium and investigated autotrophic nitrate-reducing Fe(II)-oxidizing culture KS for 24 days. We analysed Fe- and N-speciation, cell-mineral associations, and the identity of minerals. Results were compared to batch systems (50 and 700 mL—static/shaken). The Fe(II) oxidation rate was highest in the chemostat with 7.57 mM Fe(II) d−1, while the extent of oxidation was similar to the other experimental setups (average oxidation of 92% of all Fe(II)). Short-range ordered Fe(III) phases, presumably ferrihydrite, precipitated and later goethite was detected in the chemostat. The 1 mM solid phase Fe(II) remained in the chemostat, up to 15 μM of reactive nitrite was measured, and 42% of visualized cells were partially or completely mineral-encrusted, likely caused by abiotic oxidation of Fe(II) by nitrite. Despite (partial) encrustation, cells were still viable. Our results show that even with similar oxidation rates as in batch cultures, cultivating Fe(II)-oxidizing microorganisms under continuous conditions reveals the importance of reactive nitrogen intermediates on Fe(II) oxidation, mineral formation and cell–mineral interactions.",

author = "Timm Bayer and Tomaszewski, {Elizabeth J.} and Casey Bryce and Andreas Kappler and Byrne, {James M.}",

note = "Funding Information: The authors thank Natalia Jakus for μ-XRD measurements and help with sample analysis. Markus Turad and Ronny L{\"o}ffler (LISA+, University of T{\"u}bingen) for access to and help with scanning electron microscopy as well as Hartmut Schulz for help with scanning electron microscopy. Julian Sorwat and Manuel Schad for M{\"o}ssbauer measurements. Lars Grimm for help with cultivation of culture KS. The authors acknowledge APS for XAS measurements: MRCAT operations are supported by the Department of Energy and the MRCAT member institutions. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. The authors acknowledge funding from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; BY 82/2-1) awarded to J. M. Byrne as well as infrastructural support by the DFG under Germany's Excellence Strategy, cluster of Excellence EXC2124, project ID 390838134. The authors also thank UK Research and Innovation for providing the grant: MR/V023918/1. Funding Information: The authors thank Natalia Jakus for μ‐XRD measurements and help with sample analysis. Markus Turad and Ronny L{\"o}ffler (LISA, University of T{\"u}bingen) for access to and help with scanning electron microscopy as well as Hartmut Schulz for help with scanning electron microscopy. Julian Sorwat and Manuel Schad for M{\"o}ssbauer measurements. Lars Grimm for help with cultivation of culture KS. The authors acknowledge APS for XAS measurements: MRCAT operations are supported by the Department of Energy and the MRCAT member institutions. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE‐AC02‐06CH11357. The authors acknowledge funding from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; BY 82/2‐1) awarded to J. M. Byrne as well as infrastructural support by the DFG under Germany's Excellence Strategy, cluster of Excellence EXC2124, project ID 390838134. The authors also thank UK Research and Innovation for providing the grant: MR/V023918/1. + Publisher Copyright: {\textcopyright} 2023 The Authors. Environmental Microbiology Reports published by Applied Microbiology International and John Wiley & Sons Ltd.",

year = "2023",

month = mar,

day = "29",

doi = "10.1111/1758-2229.13149",

language = "English",

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T1 - Continuous cultivation of the lithoautotrophic nitrate‐reducing Fe( II )‐oxidizing culture KS in a chemostat bioreactor

AU - Bayer, Timm

AU - Tomaszewski, Elizabeth J.

AU - Bryce, Casey

AU - Kappler, Andreas

AU - Byrne, James M.

N1 - Funding Information: The authors thank Natalia Jakus for μ-XRD measurements and help with sample analysis. Markus Turad and Ronny Löffler (LISA+, University of Tübingen) for access to and help with scanning electron microscopy as well as Hartmut Schulz for help with scanning electron microscopy. Julian Sorwat and Manuel Schad for Mössbauer measurements. Lars Grimm for help with cultivation of culture KS. The authors acknowledge APS for XAS measurements: MRCAT operations are supported by the Department of Energy and the MRCAT member institutions. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. The authors acknowledge funding from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; BY 82/2-1) awarded to J. M. Byrne as well as infrastructural support by the DFG under Germany's Excellence Strategy, cluster of Excellence EXC2124, project ID 390838134. The authors also thank UK Research and Innovation for providing the grant: MR/V023918/1. Funding Information: The authors thank Natalia Jakus for μ‐XRD measurements and help with sample analysis. Markus Turad and Ronny Löffler (LISA, University of Tübingen) for access to and help with scanning electron microscopy as well as Hartmut Schulz for help with scanning electron microscopy. Julian Sorwat and Manuel Schad for Mössbauer measurements. Lars Grimm for help with cultivation of culture KS. The authors acknowledge APS for XAS measurements: MRCAT operations are supported by the Department of Energy and the MRCAT member institutions. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE‐AC02‐06CH11357. The authors acknowledge funding from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; BY 82/2‐1) awarded to J. M. Byrne as well as infrastructural support by the DFG under Germany's Excellence Strategy, cluster of Excellence EXC2124, project ID 390838134. The authors also thank UK Research and Innovation for providing the grant: MR/V023918/1. + Publisher Copyright: © 2023 The Authors. Environmental Microbiology Reports published by Applied Microbiology International and John Wiley & Sons Ltd.

PY - 2023/3/29

Y1 - 2023/3/29

N2 - Laboratory-based studies on microbial Fe(II) oxidation are commonly performed for 5–10 days in small volumes with high substrate concentrations, resulting in geochemical gradients and volumetric effects caused by sampling. We used a chemostat to enable uninterrupted supply of medium and investigated autotrophic nitrate-reducing Fe(II)-oxidizing culture KS for 24 days. We analysed Fe- and N-speciation, cell-mineral associations, and the identity of minerals. Results were compared to batch systems (50 and 700 mL—static/shaken). The Fe(II) oxidation rate was highest in the chemostat with 7.57 mM Fe(II) d−1, while the extent of oxidation was similar to the other experimental setups (average oxidation of 92% of all Fe(II)). Short-range ordered Fe(III) phases, presumably ferrihydrite, precipitated and later goethite was detected in the chemostat. The 1 mM solid phase Fe(II) remained in the chemostat, up to 15 μM of reactive nitrite was measured, and 42% of visualized cells were partially or completely mineral-encrusted, likely caused by abiotic oxidation of Fe(II) by nitrite. Despite (partial) encrustation, cells were still viable. Our results show that even with similar oxidation rates as in batch cultures, cultivating Fe(II)-oxidizing microorganisms under continuous conditions reveals the importance of reactive nitrogen intermediates on Fe(II) oxidation, mineral formation and cell–mineral interactions.

AB - Laboratory-based studies on microbial Fe(II) oxidation are commonly performed for 5–10 days in small volumes with high substrate concentrations, resulting in geochemical gradients and volumetric effects caused by sampling. We used a chemostat to enable uninterrupted supply of medium and investigated autotrophic nitrate-reducing Fe(II)-oxidizing culture KS for 24 days. We analysed Fe- and N-speciation, cell-mineral associations, and the identity of minerals. Results were compared to batch systems (50 and 700 mL—static/shaken). The Fe(II) oxidation rate was highest in the chemostat with 7.57 mM Fe(II) d−1, while the extent of oxidation was similar to the other experimental setups (average oxidation of 92% of all Fe(II)). Short-range ordered Fe(III) phases, presumably ferrihydrite, precipitated and later goethite was detected in the chemostat. The 1 mM solid phase Fe(II) remained in the chemostat, up to 15 μM of reactive nitrite was measured, and 42% of visualized cells were partially or completely mineral-encrusted, likely caused by abiotic oxidation of Fe(II) by nitrite. Despite (partial) encrustation, cells were still viable. Our results show that even with similar oxidation rates as in batch cultures, cultivating Fe(II)-oxidizing microorganisms under continuous conditions reveals the importance of reactive nitrogen intermediates on Fe(II) oxidation, mineral formation and cell–mineral interactions.

UR - https://doi.org/10.1111/1758-2229.13149

U2 - 10.1111/1758-2229.13149

DO - 10.1111/1758-2229.13149

M3 - Article (Academic Journal)

C2 - 36992623

SN - 1758-2229

VL - 15

SP - 324

EP - 334

JO - Environmental Microbiology Reports

JF - Environmental Microbiology Reports

IS - 4

ER -

Continuous cultivation of the lithoautotrophic nitrate‐reducing Fe( II )‐oxidizing culture KS in a chemostat bioreactor

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