High biodiversity in a benzene-degrading nitrate-reducing culture is sustained by a few primary consumers

Chrats Melkonian; Lucas Fillinger; Siavash Atashgahi; Ulisses Nunes da Rocha; Esther Kuiper; Brett Olivier; Martin Braster; Willi Gottstein; Rick Helmus; John R. Parsons; Hauke Smidt; Marcelle van der Waals; Jan Gerritse; Bernd W. Brandt; Wilfred F.M. Röling; Douwe Molenaar; Rob J.M. van Spanning

doi:10.1038/s42003-021-01948-y

High biodiversity in a benzene-degrading nitrate-reducing culture is sustained by a few primary consumers

Chrats Melkonian^*, Lucas Fillinger, Siavash Atashgahi, Ulisses Nunes da Rocha, Esther Kuiper, Brett Olivier, Martin Braster, Willi Gottstein, Rick Helmus, John R. Parsons, Hauke Smidt, Marcelle van der Waals, Jan Gerritse, Bernd W. Brandt, Wilfred F.M. Röling, Douwe Molenaar, Rob J.M. van Spanning

^*Corresponding author for this work

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

Abstract

A key question in microbial ecology is what the driving forces behind the persistence of large biodiversity in natural environments are. We studied a microbial community with more than 100 different types of species which evolved in a 15-years old bioreactor with benzene as the main carbon and energy source and nitrate as the electron acceptor. Using genome-centric metagenomics plus metatranscriptomics, we demonstrate that most of the community members likely feed on metabolic left-overs or on necromass while only a few of them, from families Rhodocyclaceae and Peptococcaceae, are candidates to degrade benzene. We verify with an additional succession experiment using metabolomics and metabarcoding that these few community members are the actual drivers of benzene degradation. As such, we hypothesize that high species richness is maintained and the complexity of a natural community is stabilized in a controlled environment by the interdependencies between the few benzene degraders and the rest of the community members, ultimately resulting in a food web with different trophic levels.

Original language	English
Article number	530
Pages (from-to)	1-12
Number of pages	12
Journal	Communications biology
Volume	4
DOIs	https://doi.org/10.1038/s42003-021-01948-y
Publication status	Published - 5 May 2021

Bibliographical note

Funding Information:
We thank Laura Luzia, Frank Bruggeman, Bas Teusink and Bastian Hornung for their significant contribution with discussions and proofreading. Evelina Tutucci, Paul Iturbe Espinoza, Philipp Savakis and Huub J. M. Op den Camp for helpful discussions. We are grateful to the late Wilfred F.M. Röling for his scientific input on experimental design. Unfortunately, he passed away before this work was published. This study was supported by a grant of BE-Basic-FES funds from the Dutch Ministry of Economic Affairs. The research of CM is supported by a Grand Solution grant from Innovation Fund Denmark (grant no. 6150-00033B), The FoodTranscriptomics project.

Publisher Copyright:
© 2021, The Author(s).

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Funding

We thank Laura Luzia, Frank Bruggeman, Bas Teusink and Bastian Hornung for their significant contribution with discussions and proofreading. Evelina Tutucci, Paul Iturbe Espinoza, Philipp Savakis and Huub J. M. Op den Camp for helpful discussions. We are grateful to the late Wilfred F.M. Röling for his scientific input on experimental design. Unfortunately, he passed away before this work was published. This study was supported by a grant of BE-Basic-FES funds from the Dutch Ministry of Economic Affairs. The research of CM is supported by a Grand Solution grant from Innovation Fund Denmark (grant no. 6150-00033B), The FoodTranscriptomics project.

Funders	Funder number
Innovationsfonden	6150-00033B
Vrije Universiteit Amsterdam
Ministerie van Economische Zaken

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https://hdl.handle.net/11245.1/57f3815c-3cc9-4c5f-8e24-79dc85fbe38e

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Melkonian, C., Fillinger, L., Atashgahi, S., da Rocha, U. N., Kuiper, E., Olivier, B., Braster, M., Gottstein, W., Helmus, R., Parsons, J. R., Smidt, H., van der Waals, M., Gerritse, J., Brandt, B. W., Röling, W. F. M., Molenaar, D., & van Spanning, R. J. M. (2021). High biodiversity in a benzene-degrading nitrate-reducing culture is sustained by a few primary consumers. Communications biology, 4, 1-12. Article 530. https://doi.org/10.1038/s42003-021-01948-y

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title = "High biodiversity in a benzene-degrading nitrate-reducing culture is sustained by a few primary consumers",

abstract = "A key question in microbial ecology is what the driving forces behind the persistence of large biodiversity in natural environments are. We studied a microbial community with more than 100 different types of species which evolved in a 15-years old bioreactor with benzene as the main carbon and energy source and nitrate as the electron acceptor. Using genome-centric metagenomics plus metatranscriptomics, we demonstrate that most of the community members likely feed on metabolic left-overs or on necromass while only a few of them, from families Rhodocyclaceae and Peptococcaceae, are candidates to degrade benzene. We verify with an additional succession experiment using metabolomics and metabarcoding that these few community members are the actual drivers of benzene degradation. As such, we hypothesize that high species richness is maintained and the complexity of a natural community is stabilized in a controlled environment by the interdependencies between the few benzene degraders and the rest of the community members, ultimately resulting in a food web with different trophic levels.",

author = "Chrats Melkonian and Lucas Fillinger and Siavash Atashgahi and {da Rocha}, {Ulisses Nunes} and Esther Kuiper and Brett Olivier and Martin Braster and Willi Gottstein and Rick Helmus and Parsons, {John R.} and Hauke Smidt and {van der Waals}, Marcelle and Jan Gerritse and Brandt, {Bernd W.} and R{\"o}ling, {Wilfred F.M.} and Douwe Molenaar and {van Spanning}, {Rob J.M.}",

note = "Funding Information: We thank Laura Luzia, Frank Bruggeman, Bas Teusink and Bastian Hornung for their significant contribution with discussions and proofreading. Evelina Tutucci, Paul Iturbe Espinoza, Philipp Savakis and Huub J. M. Op den Camp for helpful discussions. We are grateful to the late Wilfred F.M. R{\"o}ling for his scientific input on experimental design. Unfortunately, he passed away before this work was published. This study was supported by a grant of BE-Basic-FES funds from the Dutch Ministry of Economic Affairs. The research of CM is supported by a Grand Solution grant from Innovation Fund Denmark (grant no. 6150-00033B), The FoodTranscriptomics project. Publisher Copyright: {\textcopyright} 2021, The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

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Melkonian, C, Fillinger, L, Atashgahi, S, da Rocha, UN, Kuiper, E, Olivier, B, Braster, M, Gottstein, W, Helmus, R, Parsons, JR, Smidt, H, van der Waals, M, Gerritse, J, Brandt, BW, Röling, WFM, Molenaar, D & van Spanning, RJM 2021, 'High biodiversity in a benzene-degrading nitrate-reducing culture is sustained by a few primary consumers', Communications biology, vol. 4, 530, pp. 1-12. https://doi.org/10.1038/s42003-021-01948-y

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AU - Melkonian, Chrats

AU - Fillinger, Lucas

AU - Atashgahi, Siavash

AU - da Rocha, Ulisses Nunes

AU - Kuiper, Esther

AU - Olivier, Brett

AU - Braster, Martin

AU - Gottstein, Willi

AU - Helmus, Rick

AU - Parsons, John R.

AU - Smidt, Hauke

AU - van der Waals, Marcelle

AU - Gerritse, Jan

AU - Brandt, Bernd W.

AU - Röling, Wilfred F.M.

AU - Molenaar, Douwe

AU - van Spanning, Rob J.M.

N1 - Funding Information: We thank Laura Luzia, Frank Bruggeman, Bas Teusink and Bastian Hornung for their significant contribution with discussions and proofreading. Evelina Tutucci, Paul Iturbe Espinoza, Philipp Savakis and Huub J. M. Op den Camp for helpful discussions. We are grateful to the late Wilfred F.M. Röling for his scientific input on experimental design. Unfortunately, he passed away before this work was published. This study was supported by a grant of BE-Basic-FES funds from the Dutch Ministry of Economic Affairs. The research of CM is supported by a Grand Solution grant from Innovation Fund Denmark (grant no. 6150-00033B), The FoodTranscriptomics project. Publisher Copyright: © 2021, The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/5/5

Y1 - 2021/5/5

N2 - A key question in microbial ecology is what the driving forces behind the persistence of large biodiversity in natural environments are. We studied a microbial community with more than 100 different types of species which evolved in a 15-years old bioreactor with benzene as the main carbon and energy source and nitrate as the electron acceptor. Using genome-centric metagenomics plus metatranscriptomics, we demonstrate that most of the community members likely feed on metabolic left-overs or on necromass while only a few of them, from families Rhodocyclaceae and Peptococcaceae, are candidates to degrade benzene. We verify with an additional succession experiment using metabolomics and metabarcoding that these few community members are the actual drivers of benzene degradation. As such, we hypothesize that high species richness is maintained and the complexity of a natural community is stabilized in a controlled environment by the interdependencies between the few benzene degraders and the rest of the community members, ultimately resulting in a food web with different trophic levels.

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High biodiversity in a benzene-degrading nitrate-reducing culture is sustained by a few primary consumers

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