Bioactive exometabolites drive maintenance competition in simple bacterial communities
ABSTRACTDuring prolonged resource limitation, bacterial cells can persist in metabolically active states of non-growth. These maintenance periods, such as those experienced in stationary phase, can include upregulation of secondary metabolism and release of exometabolites into the local environment....
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-04-01
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| Series: | mSystems |
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| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00064-24 |
| _version_ | 1797205190757056512 |
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| author | John L. Chodkowski Ashley Shade |
| author_facet | John L. Chodkowski Ashley Shade |
| author_sort | John L. Chodkowski |
| collection | DOAJ |
| description | ABSTRACTDuring prolonged resource limitation, bacterial cells can persist in metabolically active states of non-growth. These maintenance periods, such as those experienced in stationary phase, can include upregulation of secondary metabolism and release of exometabolites into the local environment. As resource limitation is common in many environmental microbial habitats, we hypothesized that neighboring bacterial populations employ exometabolites to compete or cooperate during maintenance and that these exometabolite-facilitated interactions can drive community outcomes. Here, we evaluated the consequences of exometabolite interactions over the stationary phase among three environmental strains: Burkholderia thailandensis E264, Chromobacterium subtsugae ATCC 31532, and Pseudomonas syringae pv. tomato DC3000. We assembled them into synthetic communities that only permitted chemical interactions. We compared the responses (transcripts) and outputs (exometabolites) of each member with and without neighbors. We found that transcriptional dynamics were changed with different neighbors and that some of these changes were coordinated between members. The dominant competitor B. thailandensis consistently upregulated biosynthetic gene clusters to produce bioactive exometabolites for both exploitative and interference competition. These results demonstrate that competition strategies during maintenance can contribute to community-level outcomes. It also suggests that the traditional concept of defining competitiveness by growth outcomes may be narrow and that maintenance competition could be an additional or alternative measure.IMPORTANCEFree-living microbial populations often persist and engage in environments that offer few or inconsistently available resources. Thus, it is important to investigate microbial interactions in this common and ecologically relevant condition of non-growth. This work investigates the consequences of resource limitation for community metabolic output and for population interactions in simple synthetic bacterial communities. Despite non-growth, we observed active, exometabolite-mediated competition among the bacterial populations. Many of these interactions and produced exometabolites were dependent on the community composition but we also observed that one dominant competitor consistently produced interfering exometabolites regardless. These results are important for predicting and understanding microbial interactions in resource-limited environments. |
| first_indexed | 2024-04-24T08:47:11Z |
| format | Article |
| id | doaj.art-0537254c17e44c769a351d670a4352ce |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-24T08:47:11Z |
| publishDate | 2024-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-0537254c17e44c769a351d670a4352ce2024-04-16T13:00:55ZengAmerican Society for MicrobiologymSystems2379-50772024-04-019410.1128/msystems.00064-24Bioactive exometabolites drive maintenance competition in simple bacterial communitiesJohn L. Chodkowski0Ashley Shade1Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USAUniversite Claude Bernard Lyon 1, Laboratoire d'Ecologie Microbienne, UMR CNRS 5557, UMR INRAE 1418, VetAgro Sup, Villeurbanne, FranceABSTRACTDuring prolonged resource limitation, bacterial cells can persist in metabolically active states of non-growth. These maintenance periods, such as those experienced in stationary phase, can include upregulation of secondary metabolism and release of exometabolites into the local environment. As resource limitation is common in many environmental microbial habitats, we hypothesized that neighboring bacterial populations employ exometabolites to compete or cooperate during maintenance and that these exometabolite-facilitated interactions can drive community outcomes. Here, we evaluated the consequences of exometabolite interactions over the stationary phase among three environmental strains: Burkholderia thailandensis E264, Chromobacterium subtsugae ATCC 31532, and Pseudomonas syringae pv. tomato DC3000. We assembled them into synthetic communities that only permitted chemical interactions. We compared the responses (transcripts) and outputs (exometabolites) of each member with and without neighbors. We found that transcriptional dynamics were changed with different neighbors and that some of these changes were coordinated between members. The dominant competitor B. thailandensis consistently upregulated biosynthetic gene clusters to produce bioactive exometabolites for both exploitative and interference competition. These results demonstrate that competition strategies during maintenance can contribute to community-level outcomes. It also suggests that the traditional concept of defining competitiveness by growth outcomes may be narrow and that maintenance competition could be an additional or alternative measure.IMPORTANCEFree-living microbial populations often persist and engage in environments that offer few or inconsistently available resources. Thus, it is important to investigate microbial interactions in this common and ecologically relevant condition of non-growth. This work investigates the consequences of resource limitation for community metabolic output and for population interactions in simple synthetic bacterial communities. Despite non-growth, we observed active, exometabolite-mediated competition among the bacterial populations. Many of these interactions and produced exometabolites were dependent on the community composition but we also observed that one dominant competitor consistently produced interfering exometabolites regardless. These results are important for predicting and understanding microbial interactions in resource-limited environments.https://journals.asm.org/doi/10.1128/msystems.00064-24antibiotic productionbiosynthetic gene clustersBurkholderiaChromobacteriumPseudomonasDC3000 |
| spellingShingle | John L. Chodkowski Ashley Shade Bioactive exometabolites drive maintenance competition in simple bacterial communities mSystems antibiotic production biosynthetic gene clusters Burkholderia Chromobacterium Pseudomonas DC3000 |
| title | Bioactive exometabolites drive maintenance competition in simple bacterial communities |
| title_full | Bioactive exometabolites drive maintenance competition in simple bacterial communities |
| title_fullStr | Bioactive exometabolites drive maintenance competition in simple bacterial communities |
| title_full_unstemmed | Bioactive exometabolites drive maintenance competition in simple bacterial communities |
| title_short | Bioactive exometabolites drive maintenance competition in simple bacterial communities |
| title_sort | bioactive exometabolites drive maintenance competition in simple bacterial communities |
| topic | antibiotic production biosynthetic gene clusters Burkholderia Chromobacterium Pseudomonas DC3000 |
| url | https://journals.asm.org/doi/10.1128/msystems.00064-24 |
| work_keys_str_mv | AT johnlchodkowski bioactiveexometabolitesdrivemaintenancecompetitioninsimplebacterialcommunities AT ashleyshade bioactiveexometabolitesdrivemaintenancecompetitioninsimplebacterialcommunities |