In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial Mat
<i>Chloroflexus aggregans</i> is a metabolically versatile, thermophilic, anoxygenic phototrophic member of the phylum <i>Chloroflexota</i> (formerly <i>Chloroflexi</i>), which can grow photoheterotrophically, photoautotrophically, chemoheterotrophically, and chem...
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MDPI AG
2021-03-01
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| author | Shigeru Kawai Joval N. Martinez Mads Lichtenberg Erik Trampe Michael Kühl Marcus Tank Shin Haruta Arisa Nishihara Satoshi Hanada Vera Thiel |
| author_facet | Shigeru Kawai Joval N. Martinez Mads Lichtenberg Erik Trampe Michael Kühl Marcus Tank Shin Haruta Arisa Nishihara Satoshi Hanada Vera Thiel |
| author_sort | Shigeru Kawai |
| collection | DOAJ |
| description | <i>Chloroflexus aggregans</i> is a metabolically versatile, thermophilic, anoxygenic phototrophic member of the phylum <i>Chloroflexota</i> (formerly <i>Chloroflexi</i>), which can grow photoheterotrophically, photoautotrophically, chemoheterotrophically, and chemoautotrophically. In hot spring-associated microbial mats, <i>C. aggregans</i> co-exists with oxygenic cyanobacteria under dynamic micro-environmental conditions. To elucidate the predominant growth modes of <i>C. aggregans</i>, relative transcription levels of energy metabolism- and CO<sub>2</sub> fixation-related genes were studied in Nakabusa Hot Springs microbial mats over a diel cycle and correlated with microscale in situ measurements of O<sub>2</sub> and light. Metatranscriptomic analyses indicated two periods with different modes of energy metabolism of <i>C. aggregans</i>: (1) phototrophy around midday and (2) chemotrophy in the early morning hours. During midday, <i>C. aggregans</i> mainly employed photoheterotrophy when the microbial mats were hyperoxic (400–800 µmol L<sup>−1</sup> O<sub>2</sub>). In the early morning hours, relative transcription peaks of genes encoding uptake hydrogenase, key enzymes for carbon fixation, respiratory complexes as well as enzymes for TCA cycle and acetate uptake suggest an aerobic chemomixotrophic lifestyle. This is the first in situ study of the versatile energy metabolism of <i>C. aggregans</i> based on gene transcription patterns. The results provide novel insights into the metabolic flexibility of these filamentous anoxygenic phototrophs that thrive under dynamic environmental conditions. |
| first_indexed | 2024-03-10T13:01:55Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T13:01:55Z |
| publishDate | 2021-03-01 |
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| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-26c26ece00d640719823dfb400d449072023-11-21T11:24:27ZengMDPI AGMicroorganisms2076-26072021-03-019365210.3390/microorganisms9030652In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial MatShigeru Kawai0Joval N. Martinez1Mads Lichtenberg2Erik Trampe3Michael Kühl4Marcus Tank5Shin Haruta6Arisa Nishihara7Satoshi Hanada8Vera Thiel9Department of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, JapanDepartment of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, JapanDepartment of Biology, Marine Biological Section, University of Copenhagen, Strandpromenaden 5, 3000 Helsingør, DenmarkDepartment of Biology, Marine Biological Section, University of Copenhagen, Strandpromenaden 5, 3000 Helsingør, DenmarkDepartment of Biology, Marine Biological Section, University of Copenhagen, Strandpromenaden 5, 3000 Helsingør, DenmarkDepartment of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, JapanDepartment of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, JapanDepartment of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, JapanDepartment of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, JapanDepartment of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, Japan<i>Chloroflexus aggregans</i> is a metabolically versatile, thermophilic, anoxygenic phototrophic member of the phylum <i>Chloroflexota</i> (formerly <i>Chloroflexi</i>), which can grow photoheterotrophically, photoautotrophically, chemoheterotrophically, and chemoautotrophically. In hot spring-associated microbial mats, <i>C. aggregans</i> co-exists with oxygenic cyanobacteria under dynamic micro-environmental conditions. To elucidate the predominant growth modes of <i>C. aggregans</i>, relative transcription levels of energy metabolism- and CO<sub>2</sub> fixation-related genes were studied in Nakabusa Hot Springs microbial mats over a diel cycle and correlated with microscale in situ measurements of O<sub>2</sub> and light. Metatranscriptomic analyses indicated two periods with different modes of energy metabolism of <i>C. aggregans</i>: (1) phototrophy around midday and (2) chemotrophy in the early morning hours. During midday, <i>C. aggregans</i> mainly employed photoheterotrophy when the microbial mats were hyperoxic (400–800 µmol L<sup>−1</sup> O<sub>2</sub>). In the early morning hours, relative transcription peaks of genes encoding uptake hydrogenase, key enzymes for carbon fixation, respiratory complexes as well as enzymes for TCA cycle and acetate uptake suggest an aerobic chemomixotrophic lifestyle. This is the first in situ study of the versatile energy metabolism of <i>C. aggregans</i> based on gene transcription patterns. The results provide novel insights into the metabolic flexibility of these filamentous anoxygenic phototrophs that thrive under dynamic environmental conditions.https://www.mdpi.com/2076-2607/9/3/652filamentous anoxygenic phototrophmicrobial matshot springsmetatranscriptomicsenergy metabolismcarbon fixation |
| spellingShingle | Shigeru Kawai Joval N. Martinez Mads Lichtenberg Erik Trampe Michael Kühl Marcus Tank Shin Haruta Arisa Nishihara Satoshi Hanada Vera Thiel In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial Mat Microorganisms filamentous anoxygenic phototroph microbial mats hot springs metatranscriptomics energy metabolism carbon fixation |
| title | In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial Mat |
| title_full | In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial Mat |
| title_fullStr | In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial Mat |
| title_full_unstemmed | In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial Mat |
| title_short | In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium <i>Chloroflexus aggregans</i> in a Hot Spring Cyanobacteria-Dominated Microbial Mat |
| title_sort | in situ metatranscriptomic analyses reveal the metabolic flexibility of the thermophilic anoxygenic photosynthetic bacterium i chloroflexus aggregans i in a hot spring cyanobacteria dominated microbial mat |
| topic | filamentous anoxygenic phototroph microbial mats hot springs metatranscriptomics energy metabolism carbon fixation |
| url | https://www.mdpi.com/2076-2607/9/3/652 |
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