The phylogeny of Acetobacteraceae: photosynthetic traits and deranged respiratory enzymes
ABSTRACT We present here a comprehensive phylogenomic analysis of Acetobacteraceae, a vast group of alphaproteobacteria that has been widely studied for their economic importance. Our results indicate that the ancestor of Acetobacteraceae most likely was photosynthetic and evolved via a progressive...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00575-23 |
| _version_ | 1797393612070191104 |
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| author | Mauro Degli Esposti Gabriela Guerrero Marco A. Rogel Francisco Issotta Camila Rojas-Villalobos Raquel Quatrini Esperanza Martinez-Romero |
| author_facet | Mauro Degli Esposti Gabriela Guerrero Marco A. Rogel Francisco Issotta Camila Rojas-Villalobos Raquel Quatrini Esperanza Martinez-Romero |
| author_sort | Mauro Degli Esposti |
| collection | DOAJ |
| description | ABSTRACT We present here a comprehensive phylogenomic analysis of Acetobacteraceae, a vast group of alphaproteobacteria that has been widely studied for their economic importance. Our results indicate that the ancestor of Acetobacteraceae most likely was photosynthetic and evolved via a progressive transition from versatile photoferrotrophy to the incomplete oxidation of organic substrates defining acetous physiology. Vestigial signs of photosynthetic carotenoid metabolism are present in non-photosynthetic acetous taxa that have lost cytochrome oxidase, while their sister taxa retain such traits. The dominant terminal oxidase of acetous bacteria, the bo 3 ubiquinol oxidase, is derived from duplication and diversification of operons present in Acidocella taxa that have lost photosynthesis. We analyzed the bioenergetic traits that can compensate for the electron transfer function of photosynthetic reaction centers or constitute alternative pathways for the oxidoreduction of c-type cytochromes, such as iron oxidation. The latter pathway bypasses the deranged cytochrome bc 1 complex that is characteristically present in acidophilic taxa due to the loss of conserved ligands in both the Rieske iron-sulfur protein and cytochrome b subunit. The deranged or non-functional bc 1 complex may be retained for its structural role in stabilizing Complex I. The combination of our phylogenetic analysis with in-depth functional evaluations indicates that the order Acetobacterales needs to be emended to include three families: Acetobacteraceae sensu stricto, Roseomonadaceae fam. nov., and Acidocellaceae fam. nov. IMPORTANCE Acetobacteraceae are one of the best known and most extensively studied groups of bacteria, which nowadays encompasses a variety of taxa that are very different from the vinegar-producing species defining the family. Our paper presents the most detailed phylogeny of all current taxa classified as Acetobacteraceae, for which we propose a taxonomic revision. Several of such taxa inhabit some of the most extreme environments on the planet, from the deserts of Antarctica to the Sinai desert, as well as acidic niches in volcanic sites like the one we have been studying in Patagonia. Our work documents the progressive variation of the respiratory chain in early branching Acetobacteraceae into the different respiratory chains of acidophilic taxa such as Acidocella and acetous taxa such as Acetobacter. Remarkably, several genomes retain remnants of ancestral photosynthetic traits and functional bc 1 complexes. Thus, we propose that the common ancestor of Acetobacteraceae was photosynthetic. |
| first_indexed | 2024-03-09T00:06:22Z |
| format | Article |
| id | doaj.art-895c69c9adf84e578a4cb4129aec8c10 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:06:22Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-895c69c9adf84e578a4cb4129aec8c102023-12-12T13:17:20ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.00575-23The phylogeny of Acetobacteraceae: photosynthetic traits and deranged respiratory enzymesMauro Degli Esposti0Gabriela Guerrero1Marco A. Rogel2Francisco Issotta3Camila Rojas-Villalobos4Raquel Quatrini5Esperanza Martinez-Romero6Center for Genomic Sciences, UNAM Campus de Morelos , Cuernavaca, Morelos, MexicoCenter for Genomic Sciences, UNAM Campus de Morelos , Cuernavaca, Morelos, MexicoCenter for Genomic Sciences, UNAM Campus de Morelos , Cuernavaca, Morelos, MexicoCentro Científico y Tecnológico de Excelencia Ciencia & Vida, Fundación Ciencia y Vida , Huechuraba, Santiago, ChileCentro Científico y Tecnológico de Excelencia Ciencia & Vida, Fundación Ciencia y Vida , Huechuraba, Santiago, ChileCentro Científico y Tecnológico de Excelencia Ciencia & Vida, Fundación Ciencia y Vida , Huechuraba, Santiago, ChileCenter for Genomic Sciences, UNAM Campus de Morelos , Cuernavaca, Morelos, MexicoABSTRACT We present here a comprehensive phylogenomic analysis of Acetobacteraceae, a vast group of alphaproteobacteria that has been widely studied for their economic importance. Our results indicate that the ancestor of Acetobacteraceae most likely was photosynthetic and evolved via a progressive transition from versatile photoferrotrophy to the incomplete oxidation of organic substrates defining acetous physiology. Vestigial signs of photosynthetic carotenoid metabolism are present in non-photosynthetic acetous taxa that have lost cytochrome oxidase, while their sister taxa retain such traits. The dominant terminal oxidase of acetous bacteria, the bo 3 ubiquinol oxidase, is derived from duplication and diversification of operons present in Acidocella taxa that have lost photosynthesis. We analyzed the bioenergetic traits that can compensate for the electron transfer function of photosynthetic reaction centers or constitute alternative pathways for the oxidoreduction of c-type cytochromes, such as iron oxidation. The latter pathway bypasses the deranged cytochrome bc 1 complex that is characteristically present in acidophilic taxa due to the loss of conserved ligands in both the Rieske iron-sulfur protein and cytochrome b subunit. The deranged or non-functional bc 1 complex may be retained for its structural role in stabilizing Complex I. The combination of our phylogenetic analysis with in-depth functional evaluations indicates that the order Acetobacterales needs to be emended to include three families: Acetobacteraceae sensu stricto, Roseomonadaceae fam. nov., and Acidocellaceae fam. nov. IMPORTANCE Acetobacteraceae are one of the best known and most extensively studied groups of bacteria, which nowadays encompasses a variety of taxa that are very different from the vinegar-producing species defining the family. Our paper presents the most detailed phylogeny of all current taxa classified as Acetobacteraceae, for which we propose a taxonomic revision. Several of such taxa inhabit some of the most extreme environments on the planet, from the deserts of Antarctica to the Sinai desert, as well as acidic niches in volcanic sites like the one we have been studying in Patagonia. Our work documents the progressive variation of the respiratory chain in early branching Acetobacteraceae into the different respiratory chains of acidophilic taxa such as Acidocella and acetous taxa such as Acetobacter. Remarkably, several genomes retain remnants of ancestral photosynthetic traits and functional bc 1 complexes. Thus, we propose that the common ancestor of Acetobacteraceae was photosynthetic.https://journals.asm.org/doi/10.1128/spectrum.00575-23phylogenomicsbacterial phylogenyenergy metabolismAcetobacteraceae |
| spellingShingle | Mauro Degli Esposti Gabriela Guerrero Marco A. Rogel Francisco Issotta Camila Rojas-Villalobos Raquel Quatrini Esperanza Martinez-Romero The phylogeny of Acetobacteraceae: photosynthetic traits and deranged respiratory enzymes Microbiology Spectrum phylogenomics bacterial phylogeny energy metabolism Acetobacteraceae |
| title | The phylogeny of Acetobacteraceae: photosynthetic traits and deranged respiratory enzymes |
| title_full | The phylogeny of Acetobacteraceae: photosynthetic traits and deranged respiratory enzymes |
| title_fullStr | The phylogeny of Acetobacteraceae: photosynthetic traits and deranged respiratory enzymes |
| title_full_unstemmed | The phylogeny of Acetobacteraceae: photosynthetic traits and deranged respiratory enzymes |
| title_short | The phylogeny of Acetobacteraceae: photosynthetic traits and deranged respiratory enzymes |
| title_sort | phylogeny of acetobacteraceae photosynthetic traits and deranged respiratory enzymes |
| topic | phylogenomics bacterial phylogeny energy metabolism Acetobacteraceae |
| url | https://journals.asm.org/doi/10.1128/spectrum.00575-23 |
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