A thermophilic chemolithoautotrophic bacterial consortium suggests a mutual relationship between bacteria in extreme oligotrophic environments

Yuri Pinheiro; Fabio Faria da Mota; Raquel S Peixoto; Jan Dirk van Elsas; Ulysses Lins; Jorge L. Mazza Rodrigues; Alexandre S. Rosado

doi:10.1038/s42003-023-04617-4

A thermophilic chemolithoautotrophic bacterial consortium suggests a mutual relationship between bacteria in extreme oligotrophic environments

Yuri Pinheiro, Fabio Faria da Mota, Raquel S Peixoto, Jan Dirk van Elsas, Ulysses Lins, Jorge L. Mazza Rodrigues, Alexandre S. Rosado

Research output: Contribution to journal › Article › peer-review

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Abstract

A thermophilic, chemolithoautotrophic, and aerobic microbial consortium (termed carbonitroflex) growing in a nutrient-poor medium and an atmosphere containing N2, O2, CO2, and CO is investigated as a model to expand our understanding of extreme biological systems. Here we show that the consortium is dominated by Carbonactinospora thermoautotrophica (strain StC), followed by Sphaerobacter thermophilus, Chelatococcus spp., and Geobacillus spp. Metagenomic analysis of the consortium reveals a mutual relationship among bacteria, with C. thermoautotrophica StC exhibiting carboxydotrophy and carbon-dioxide storage capacity. C. thermoautotrophica StC, Chelatococcus spp., and S. thermophilus harbor genes encoding CO dehydrogenase and formate oxidase. No pure cultures were obtained under the original growth conditions, indicating that a tightly regulated interactive metabolism might be required for group survival and growth in this extreme oligotrophic system. The breadwinner hypothesis is proposed to explain the metabolic flux model and highlight the vital role of C. thermoautotrophica StC (the sole keystone species and primary carbon producer) in the survival of all consortium members. Our data may contribute to the investigation of complex interactions in extreme environments, exemplifying the interconnections and dependency within microbial communities.

Original language	English (US)
Journal	Communications Biology
Volume	6
Issue number	1
DOIs	https://doi.org/10.1038/s42003-023-04617-4
State	Published - Mar 1 2023

Bibliographical note

KAUST Repository Item: Exported on 2023-03-07
Acknowledged KAUST grant number(s): BAS/1/1096-01-01
Acknowledgements: This research was financially supported by the National Council for Research and Development (CNPq), the National Council for the Improvement of Higher Education (CAPES), and a KAUST Baseline Grant (to Prof. A. S. Rosado) (BAS/1/1096-01-01). We thank Edir Martins Ferreira and Tahira Jamil for their excellent technical assistance and Prof. E. Zonta for soil analysis. We would like to remember Professor Ulysses Lins, who is sadly no longer with us and to whom we owe much more than words.

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10.1038/s42003-023-04617-4

https://repository.kaust.edu.sa/bitstream/10754/690111/1/s42003-023-04617-4.pdf

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title = "A thermophilic chemolithoautotrophic bacterial consortium suggests a mutual relationship between bacteria in extreme oligotrophic environments",

abstract = "A thermophilic, chemolithoautotrophic, and aerobic microbial consortium (termed carbonitroflex) growing in a nutrient-poor medium and an atmosphere containing N2, O2, CO2, and CO is investigated as a model to expand our understanding of extreme biological systems. Here we show that the consortium is dominated by Carbonactinospora thermoautotrophica (strain StC), followed by Sphaerobacter thermophilus, Chelatococcus spp., and Geobacillus spp. Metagenomic analysis of the consortium reveals a mutual relationship among bacteria, with C. thermoautotrophica StC exhibiting carboxydotrophy and carbon-dioxide storage capacity. C. thermoautotrophica StC, Chelatococcus spp., and S. thermophilus harbor genes encoding CO dehydrogenase and formate oxidase. No pure cultures were obtained under the original growth conditions, indicating that a tightly regulated interactive metabolism might be required for group survival and growth in this extreme oligotrophic system. The breadwinner hypothesis is proposed to explain the metabolic flux model and highlight the vital role of C. thermoautotrophica StC (the sole keystone species and primary carbon producer) in the survival of all consortium members. Our data may contribute to the investigation of complex interactions in extreme environments, exemplifying the interconnections and dependency within microbial communities.",

author = "Yuri Pinheiro and {Faria da Mota}, Fabio and Peixoto, {Raquel S} and {van Elsas}, {Jan Dirk} and Ulysses Lins and Rodrigues, {Jorge L. Mazza} and Rosado, {Alexandre S.}",

note = "KAUST Repository Item: Exported on 2023-03-07 Acknowledged KAUST grant number(s): BAS/1/1096-01-01 Acknowledgements: This research was financially supported by the National Council for Research and Development (CNPq), the National Council for the Improvement of Higher Education (CAPES), and a KAUST Baseline Grant (to Prof. A. S. Rosado) (BAS/1/1096-01-01). We thank Edir Martins Ferreira and Tahira Jamil for their excellent technical assistance and Prof. E. Zonta for soil analysis. We would like to remember Professor Ulysses Lins, who is sadly no longer with us and to whom we owe much more than words.",

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doi = "10.1038/s42003-023-04617-4",

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AU - Pinheiro, Yuri

AU - Faria da Mota, Fabio

AU - Peixoto, Raquel S

AU - van Elsas, Jan Dirk

AU - Lins, Ulysses

AU - Rodrigues, Jorge L. Mazza

AU - Rosado, Alexandre S.

N1 - KAUST Repository Item: Exported on 2023-03-07 Acknowledged KAUST grant number(s): BAS/1/1096-01-01 Acknowledgements: This research was financially supported by the National Council for Research and Development (CNPq), the National Council for the Improvement of Higher Education (CAPES), and a KAUST Baseline Grant (to Prof. A. S. Rosado) (BAS/1/1096-01-01). We thank Edir Martins Ferreira and Tahira Jamil for their excellent technical assistance and Prof. E. Zonta for soil analysis. We would like to remember Professor Ulysses Lins, who is sadly no longer with us and to whom we owe much more than words.

PY - 2023/3/1

Y1 - 2023/3/1

N2 - A thermophilic, chemolithoautotrophic, and aerobic microbial consortium (termed carbonitroflex) growing in a nutrient-poor medium and an atmosphere containing N2, O2, CO2, and CO is investigated as a model to expand our understanding of extreme biological systems. Here we show that the consortium is dominated by Carbonactinospora thermoautotrophica (strain StC), followed by Sphaerobacter thermophilus, Chelatococcus spp., and Geobacillus spp. Metagenomic analysis of the consortium reveals a mutual relationship among bacteria, with C. thermoautotrophica StC exhibiting carboxydotrophy and carbon-dioxide storage capacity. C. thermoautotrophica StC, Chelatococcus spp., and S. thermophilus harbor genes encoding CO dehydrogenase and formate oxidase. No pure cultures were obtained under the original growth conditions, indicating that a tightly regulated interactive metabolism might be required for group survival and growth in this extreme oligotrophic system. The breadwinner hypothesis is proposed to explain the metabolic flux model and highlight the vital role of C. thermoautotrophica StC (the sole keystone species and primary carbon producer) in the survival of all consortium members. Our data may contribute to the investigation of complex interactions in extreme environments, exemplifying the interconnections and dependency within microbial communities.

AB - A thermophilic, chemolithoautotrophic, and aerobic microbial consortium (termed carbonitroflex) growing in a nutrient-poor medium and an atmosphere containing N2, O2, CO2, and CO is investigated as a model to expand our understanding of extreme biological systems. Here we show that the consortium is dominated by Carbonactinospora thermoautotrophica (strain StC), followed by Sphaerobacter thermophilus, Chelatococcus spp., and Geobacillus spp. Metagenomic analysis of the consortium reveals a mutual relationship among bacteria, with C. thermoautotrophica StC exhibiting carboxydotrophy and carbon-dioxide storage capacity. C. thermoautotrophica StC, Chelatococcus spp., and S. thermophilus harbor genes encoding CO dehydrogenase and formate oxidase. No pure cultures were obtained under the original growth conditions, indicating that a tightly regulated interactive metabolism might be required for group survival and growth in this extreme oligotrophic system. The breadwinner hypothesis is proposed to explain the metabolic flux model and highlight the vital role of C. thermoautotrophica StC (the sole keystone species and primary carbon producer) in the survival of all consortium members. Our data may contribute to the investigation of complex interactions in extreme environments, exemplifying the interconnections and dependency within microbial communities.

UR - http://hdl.handle.net/10754/690111

UR - https://www.nature.com/articles/s42003-023-04617-4

U2 - 10.1038/s42003-023-04617-4

DO - 10.1038/s42003-023-04617-4

M3 - Article

C2 - 36859706

SN - 2399-3642

VL - 6

JO - Communications Biology

JF - Communications Biology

IS - 1

ER -

A thermophilic chemolithoautotrophic bacterial consortium suggests a mutual relationship between bacteria in extreme oligotrophic environments

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