Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilis

ABSTRACT Microbial community analysis of aquatic environments showed that an important component of its microbial diversity consists of bacteria with cell sizes of ~0.1 μm. Such small bacteria can show genomic reductions and metabolic dependencies with other bacteria. However, so far, no study has i...

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Main Authors: Olaf Tyc, Purva Kulkarni, Adam Ossowicki, Vittorio Tracanna, Marnix H. Medema, Peter van Baarlen, W. F. J. van IJcken, Koen J. F. Verhoeven, Paolina Garbeva
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語言:英语
出版: American Society for Microbiology 2023-02-01
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在線閱讀:https://journals.asm.org/doi/10.1128/msystems.00574-22
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author Olaf Tyc
Purva Kulkarni
Adam Ossowicki
Vittorio Tracanna
Marnix H. Medema
Peter van Baarlen
W. F. J. van IJcken
Koen J. F. Verhoeven
Paolina Garbeva
author_facet Olaf Tyc
Purva Kulkarni
Adam Ossowicki
Vittorio Tracanna
Marnix H. Medema
Peter van Baarlen
W. F. J. van IJcken
Koen J. F. Verhoeven
Paolina Garbeva
author_sort Olaf Tyc
collection DOAJ
container_title mSystems
description ABSTRACT Microbial community analysis of aquatic environments showed that an important component of its microbial diversity consists of bacteria with cell sizes of ~0.1 μm. Such small bacteria can show genomic reductions and metabolic dependencies with other bacteria. However, so far, no study has investigated if such bacteria exist in terrestrial environments like soil. Here, we isolated soil bacteria that passed through a 0.1-μm filter. The complete genome of one of the isolates was sequenced and the bacterium was identified as Hylemonella gracilis. A set of coculture assays with phylogenetically distant soil bacteria with different cell and genome sizes was performed. The coculture assays revealed that H. gracilis grows better when interacting with other soil bacteria like Paenibacillus sp. AD87 and Serratia plymuthica. Transcriptomics and metabolomics showed that H. gracilis was able to change gene expression, behavior, and biochemistry of the interacting bacteria without direct cell-cell contact. Our study indicates that in soil there are bacteria that can pass through a 0.1-μm filter. These bacteria may have been overlooked in previous research on soil microbial communities. Such small bacteria, exemplified here by H. gracilis, can induce transcriptional and metabolomic changes in other bacteria upon their interactions in soil. In vitro, the studied interspecific interactions allowed utilization of growth substrates that could not be utilized by monocultures, suggesting that biochemical interactions between substantially different sized soil bacteria may contribute to the symbiosis of soil bacterial communities. IMPORTANCE Analysis of aquatic microbial communities revealed that parts of its diversity consist of bacteria with cell sizes of ~0.1 μm. Such bacteria can show genomic reductions and metabolic dependencies with other bacteria. So far, no study investigated if such bacteria exist in terrestrial environments such as soil. Here, we show that such bacteria also exist in soil. The isolated bacteria were identified as Hylemonella gracilis. Coculture assays with phylogenetically different soil bacteria revealed that H. gracilis grows better when cocultured with other soil bacteria. Transcriptomics and metabolomics showed that H. gracilis was able to change gene expression, behavior, and biochemistry of the interacting bacteria without direct contact. Our study revealed that bacteria are present in soil that can pass through 0.1-μm filters. Such bacteria may have been overlooked in previous research on soil microbial communities and may contribute to the symbiosis of soil bacterial communities.
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spelling doaj-art-a8e963bfcf3d4d83aa20e4b258c30feb2025-08-19T21:18:23ZengAmerican Society for MicrobiologymSystems2379-50772023-02-018110.1128/msystems.00574-22Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilisOlaf Tyc0Purva Kulkarni1Adam Ossowicki2Vittorio Tracanna3Marnix H. Medema4Peter van Baarlen5W. F. J. van IJcken6Koen J. F. Verhoeven7Paolina Garbeva8Netherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, Wageningen, NetherlandsNetherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, Wageningen, NetherlandsNetherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, Wageningen, NetherlandsWageningen University, Department of Plant Sciences, Bioinformatics Group, Wageningen, NetherlandsWageningen University, Department of Plant Sciences, Bioinformatics Group, Wageningen, NetherlandsWageningen University, Department of Animal Sciences, Host-Microbe Interactomics, Wageningen, NetherlandsCenter for Biomics, Erasmus University Medical Center, Rotterdam, NetherlandsNetherlands Institute of Ecology (NIOO-KNAW), Department of Terrestrial Ecology, Wageningen, NetherlandsNetherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, Wageningen, NetherlandsABSTRACT Microbial community analysis of aquatic environments showed that an important component of its microbial diversity consists of bacteria with cell sizes of ~0.1 μm. Such small bacteria can show genomic reductions and metabolic dependencies with other bacteria. However, so far, no study has investigated if such bacteria exist in terrestrial environments like soil. Here, we isolated soil bacteria that passed through a 0.1-μm filter. The complete genome of one of the isolates was sequenced and the bacterium was identified as Hylemonella gracilis. A set of coculture assays with phylogenetically distant soil bacteria with different cell and genome sizes was performed. The coculture assays revealed that H. gracilis grows better when interacting with other soil bacteria like Paenibacillus sp. AD87 and Serratia plymuthica. Transcriptomics and metabolomics showed that H. gracilis was able to change gene expression, behavior, and biochemistry of the interacting bacteria without direct cell-cell contact. Our study indicates that in soil there are bacteria that can pass through a 0.1-μm filter. These bacteria may have been overlooked in previous research on soil microbial communities. Such small bacteria, exemplified here by H. gracilis, can induce transcriptional and metabolomic changes in other bacteria upon their interactions in soil. In vitro, the studied interspecific interactions allowed utilization of growth substrates that could not be utilized by monocultures, suggesting that biochemical interactions between substantially different sized soil bacteria may contribute to the symbiosis of soil bacterial communities. IMPORTANCE Analysis of aquatic microbial communities revealed that parts of its diversity consist of bacteria with cell sizes of ~0.1 μm. Such bacteria can show genomic reductions and metabolic dependencies with other bacteria. So far, no study investigated if such bacteria exist in terrestrial environments such as soil. Here, we show that such bacteria also exist in soil. The isolated bacteria were identified as Hylemonella gracilis. Coculture assays with phylogenetically different soil bacteria revealed that H. gracilis grows better when cocultured with other soil bacteria. Transcriptomics and metabolomics showed that H. gracilis was able to change gene expression, behavior, and biochemistry of the interacting bacteria without direct contact. Our study revealed that bacteria are present in soil that can pass through 0.1-μm filters. Such bacteria may have been overlooked in previous research on soil microbial communities and may contribute to the symbiosis of soil bacterial communities.https://journals.asm.org/doi/10.1128/msystems.00574-22Hylemonella sp.interspecific interactionstranscriptome analysismetabolome analysisGram-negative bacteriametabolomics
spellingShingle Olaf Tyc
Purva Kulkarni
Adam Ossowicki
Vittorio Tracanna
Marnix H. Medema
Peter van Baarlen
W. F. J. van IJcken
Koen J. F. Verhoeven
Paolina Garbeva
Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilis
Hylemonella sp.
interspecific interactions
transcriptome analysis
metabolome analysis
Gram-negative bacteria
metabolomics
title Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilis
title_full Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilis
title_fullStr Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilis
title_full_unstemmed Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilis
title_short Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilis
title_sort exploring the interspecific interactions and the metabolome of the soil isolate hylemonella gracilis
topic Hylemonella sp.
interspecific interactions
transcriptome analysis
metabolome analysis
Gram-negative bacteria
metabolomics
url https://journals.asm.org/doi/10.1128/msystems.00574-22
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