Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transfer
ABSTRACT Direct interspecies electron transfer (DIET) is important in anaerobic communities of environmental and practical significance. Other than the need for close physical contact for electrical connections, the interactions of DIET partners are poorly understood. Type VI secretion systems (T6SS...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-10-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00941-23 |
| _version_ | 1797658235601158144 |
|---|---|
| author | Jessica A. Smith Dawn E. Holmes Trevor L. Woodard Yang Li Xinying Liu Li-Ying Wang David Meier Ingrid A. Schwarz Derek R. Lovley |
| author_facet | Jessica A. Smith Dawn E. Holmes Trevor L. Woodard Yang Li Xinying Liu Li-Ying Wang David Meier Ingrid A. Schwarz Derek R. Lovley |
| author_sort | Jessica A. Smith |
| collection | DOAJ |
| description | ABSTRACT Direct interspecies electron transfer (DIET) is important in anaerobic communities of environmental and practical significance. Other than the need for close physical contact for electrical connections, the interactions of DIET partners are poorly understood. Type VI secretion systems (T6SSs) typically kill competitive microbes. Surprisingly, Geobacter metallireducens highly expressed T6SS genes when DIET-based co-cultures were initiated with Geobacter sulfurreducens. T6SS gene expression was lower when the electron shuttle anthraquinone-2,6-disulfonate was added to alleviate the need for interspecies contact. Disruption of hcp, the G. metallireducens gene for the main T6SS needle-tube protein subunit, and the most highly upregulated gene in DIET-grown cells eliminated the long lag periods required for the initiation of DIET. The mutation did not aid DIET in the presence of granular-activated carbon (GAC), consistent with the fact that DIET partners do not make physical contact when electrically connected through conductive materials. The hcp-deficient mutant also established DIET quicker with Methanosarcina barkeri. However, the mutant also reduced Fe(III) oxide faster than the wild-type strain, a phenotype not expected from the loss of the T6SS. Quantitative PCR revealed greater gene transcript abundance for key components of extracellular electron transfer in the hcp-deficient mutant versus the wild-type strain, potentially accounting for the faster Fe(III) oxide reduction and impact on DIET. The results highlight that interspecies interactions beyond electrical connections may influence DIET effectiveness. The unexpected increase in the expression of genes for extracellular electron transport components when hcp was deleted emphasizes the complexities in evaluating the electromicrobiology of highly adaptable Geobacter species. IMPORTANCE Direct interspecies electron transfer is an alternative to the much more intensively studied process of interspecies H2 transfer as a mechanism for microbes to share electrons during the cooperative metabolism of energy sources. DIET is an important process in anaerobic soils and sediments generating methane, a significant greenhouse gas. Facilitating DIET can accelerate and stabilize the conversion of organic wastes to methane biofuel in anaerobic digesters. Therefore, a better understanding of the factors controlling how fast DIET partnerships are established is expected to lead to new strategies for promoting this bioenergy process. The finding that when co-cultured with G. sulfurreducens, G. metallireducens initially expressed a type VI secretion system, a behavior not conducive to interspecies cooperation, illustrates the complexity of establishing syntrophic relationships. |
| first_indexed | 2024-03-11T17:56:18Z |
| format | Article |
| id | doaj.art-97ca54eea6b64b92950d1e908f15ca94 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-11T17:56:18Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-97ca54eea6b64b92950d1e908f15ca942023-10-17T13:04:34ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-10-0111510.1128/spectrum.00941-23Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transferJessica A. Smith0Dawn E. Holmes1Trevor L. Woodard2Yang Li3Xinying Liu4Li-Ying Wang5David Meier6Ingrid A. Schwarz7Derek R. Lovley8Department of Microbiology, University of Massachusetts Amherst, Morrill IV N Science Center , Amherst, Massachusetts, USADepartment of Microbiology, University of Massachusetts Amherst, Morrill IV N Science Center , Amherst, Massachusetts, USADepartment of Microbiology, University of Massachusetts Amherst, Morrill IV N Science Center , Amherst, Massachusetts, USADepartment of Microbiology, University of Massachusetts Amherst, Morrill IV N Science Center , Amherst, Massachusetts, USADepartment of Microbiology, University of Massachusetts Amherst, Morrill IV N Science Center , Amherst, Massachusetts, USADepartment of Microbiology, University of Massachusetts Amherst, Morrill IV N Science Center , Amherst, Massachusetts, USADepartment of Microbiology, University of Massachusetts Amherst, Morrill IV N Science Center , Amherst, Massachusetts, USADepartment of Biomolecular Sciences, Central Connecticut State University , New Britain, Connecticut, USADepartment of Microbiology, University of Massachusetts Amherst, Morrill IV N Science Center , Amherst, Massachusetts, USAABSTRACT Direct interspecies electron transfer (DIET) is important in anaerobic communities of environmental and practical significance. Other than the need for close physical contact for electrical connections, the interactions of DIET partners are poorly understood. Type VI secretion systems (T6SSs) typically kill competitive microbes. Surprisingly, Geobacter metallireducens highly expressed T6SS genes when DIET-based co-cultures were initiated with Geobacter sulfurreducens. T6SS gene expression was lower when the electron shuttle anthraquinone-2,6-disulfonate was added to alleviate the need for interspecies contact. Disruption of hcp, the G. metallireducens gene for the main T6SS needle-tube protein subunit, and the most highly upregulated gene in DIET-grown cells eliminated the long lag periods required for the initiation of DIET. The mutation did not aid DIET in the presence of granular-activated carbon (GAC), consistent with the fact that DIET partners do not make physical contact when electrically connected through conductive materials. The hcp-deficient mutant also established DIET quicker with Methanosarcina barkeri. However, the mutant also reduced Fe(III) oxide faster than the wild-type strain, a phenotype not expected from the loss of the T6SS. Quantitative PCR revealed greater gene transcript abundance for key components of extracellular electron transfer in the hcp-deficient mutant versus the wild-type strain, potentially accounting for the faster Fe(III) oxide reduction and impact on DIET. The results highlight that interspecies interactions beyond electrical connections may influence DIET effectiveness. The unexpected increase in the expression of genes for extracellular electron transport components when hcp was deleted emphasizes the complexities in evaluating the electromicrobiology of highly adaptable Geobacter species. IMPORTANCE Direct interspecies electron transfer is an alternative to the much more intensively studied process of interspecies H2 transfer as a mechanism for microbes to share electrons during the cooperative metabolism of energy sources. DIET is an important process in anaerobic soils and sediments generating methane, a significant greenhouse gas. Facilitating DIET can accelerate and stabilize the conversion of organic wastes to methane biofuel in anaerobic digesters. Therefore, a better understanding of the factors controlling how fast DIET partnerships are established is expected to lead to new strategies for promoting this bioenergy process. The finding that when co-cultured with G. sulfurreducens, G. metallireducens initially expressed a type VI secretion system, a behavior not conducive to interspecies cooperation, illustrates the complexity of establishing syntrophic relationships.https://journals.asm.org/doi/10.1128/spectrum.00941-23Geobactertype VI secretion systemdirect interspecies electron transferextracellular electron transferMethanosarcina |
| spellingShingle | Jessica A. Smith Dawn E. Holmes Trevor L. Woodard Yang Li Xinying Liu Li-Ying Wang David Meier Ingrid A. Schwarz Derek R. Lovley Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transfer Microbiology Spectrum Geobacter type VI secretion system direct interspecies electron transfer extracellular electron transfer Methanosarcina |
| title | Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transfer |
| title_full | Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transfer |
| title_fullStr | Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transfer |
| title_full_unstemmed | Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transfer |
| title_short | Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transfer |
| title_sort | detrimental impact of the geobacter metallireducens type vi secretion system on direct interspecies electron transfer |
| topic | Geobacter type VI secretion system direct interspecies electron transfer extracellular electron transfer Methanosarcina |
| url | https://journals.asm.org/doi/10.1128/spectrum.00941-23 |
| work_keys_str_mv | AT jessicaasmith detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer AT dawneholmes detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer AT trevorlwoodard detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer AT yangli detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer AT xinyingliu detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer AT liyingwang detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer AT davidmeier detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer AT ingridaschwarz detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer AT derekrlovley detrimentalimpactofthegeobactermetallireducenstypevisecretionsystemondirectinterspecieselectrontransfer |