Review

Authors: Veronica Massena Reis, Kátia Regina dos Santos Teixeira

For centuries, the Acetobacteraceae is known as a family that harbors many species of organisms of biotechnological importance for industry. Nonetheless, since 1988 representatives of this family have also been described as nitrogen fixing bacteria able to plant growth promotion by a variety of mechanisms. Nitrogen fixation is a biological process that guarantees that the atmospheric N2 is incorporated into organic matter by several bacterial groups. Most representatives of this group, also known as diazotrophic, are generally associated with soil rhizosphere of many plants and also establishing a more specific association living inside roots, leaves, and others plants tissues as endophyte. Their roles as plant growth-promoting microorganisms are generally related to increase in plant biomass, phosphate and other mineral solubilization, and plant pathogen control. Here, we report many of these plant growth-promoting processes related to nitrogen fixing species already described in Acetobacteraceae family, especially Gluconacetobacter diazotrophicus and their importance to agriculture. In addition, a brief review of the state of art of the phylogenetics, main physiological and biochemical characteristics, molecular and functional genomic data of this group of Acetobacteraceae is presented.

Topics: Acetobacteraceae; Agriculture; Biomass; Endophytes; Gluconacetobacter; Nitrogen Fixation; Phylogeny; Plant Leaves; Plant Roots; Rhizosphere; Soil Microbiology

PubMed: 25736602
DOI: 10.1002/jobm.201400898

Authors: Mauro Degli Esposti, Gabriela Guerrero, Marco A Rogel...

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 , 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 and acetous taxa such as . Remarkably, several genomes retain remnants of ancestral photosynthetic traits and functional complexes. Thus, we propose that the common ancestor of was photosynthetic.

Topics: Acetobacteraceae; Phylogeny; RNA, Ribosomal, 16S; Acids; Antarctic Regions; DNA, Bacterial

PubMed: 37975678
DOI: 10.1128/spectrum.00575-23

Authors: Bryan P Brown, Jennifer J Wernegreen

BACKGROUND

Symbiotic relationships between animals and bacteria have profound impacts on the evolutionary trajectories of each partner. Animals and gut bacteria engage in a variety of relationships, occasionally persisting over evolutionary timescales. Ants are a diverse group of animals that engage in many types of associations with taxonomically distinct groups of bacterial associates. Here, we bring into culture and characterize two closely-related strains of gut associated Acetobacteraceae (AAB) of the red carpenter ant, Camponotus chromaiodes.

RESULTS

Genome sequencing, assembly, and annotation of both strains delineate stark patterns of genomic erosion and sequence divergence in gut associated AAB. We found widespread horizontal gene transfer (HGT) in these bacterial associates and report elevated gene acquisition associated with energy production and conversion, amino acid and coenzyme transport and metabolism, defense mechanisms, and lysine export. Both strains have acquired the complete NADH-quinone oxidoreductase complex, plausibly from an Enterobacteriaceae origin, likely facilitating energy production under diverse conditions. Conservation of several lysine biosynthetic and salvage pathways and accumulation of lysine export genes via HGT implicate L-lysine supplementation by both strains as a potential functional benefit for the host. These trends are contrasted by genome-wide erosion of several amino acid biosynthetic pathways and pathways in central metabolism. We perform phylogenomic analyses on both strains as well as several free living and host associated AAB. Based on their monophyly and deep divergence from other AAB, these C. chromaiodes gut associates may represent a novel genus. Together, our results demonstrate how extensive horizontal transfer between gut associates along with genome-wide deletions leads to mosaic metabolic pathways. More broadly, these patterns demonstrate that HGT and genomic erosion shape metabolic capabilities of persistent gut associates and influence their genomic evolution.

CONCLUSIONS

Using comparative genomics, our study reveals substantial changes in genomic content in persistent associates of the insect gastrointestinal tract and provides evidence for the evolutionary pressures inherent to this environment. We describe patterns of genomic erosion and horizontal acquisition that result in mosaic metabolic pathways. Accordingly, the phylogenetic position of both strains of these associates form a divergent, monophyletic clade sister to gut associates of honey bees and more distantly to Gluconobacter.

Topics: Acetobacteraceae; Animals; Ants; Evolution, Molecular; Gastrointestinal Tract; Gene Transfer, Horizontal; Genomics; Metabolic Networks and Pathways; Phylogeny; Symbiosis

PubMed: 31182035
DOI: 10.1186/s12864-019-5844-5

Authors: Juan Guzman, Andreas Vilcinskas

Acetobacteraceae is an economically important family of bacteria that is used for industrial fermentation in the food/feed sector and for the preparation of sorbose and bacterial cellulose. It comprises two major groups: acetous species (acetic acid bacteria) associated with flowers, fruits and insects, and acidophilic species, a phylogenetically basal and physiologically heterogeneous group inhabiting acid or hot springs, sludge, sewage and freshwater environments. Despite the biotechnological importance of the family Acetobacteraceae, the literature does not provide any information about its ability to produce specialized metabolites. We therefore constructed a phylogenomic tree based on concatenated protein sequences from 141 type strains of the family and predicted the presence of small-molecule biosynthetic gene clusters (BGCs) using the antiSMASH tool. This dual approach allowed us to associate certain biosynthetic pathways with particular taxonomic groups. We found that acidophilic and acetous species contain on average ~ 6.3 and ~ 3.4 BGCs per genome, respectively. All the Acetobacteraceae strains encoded proteins involved in hopanoid biosynthesis, with many also featuring genes encoding type-1 and type-3 polyketide and non-ribosomal peptide synthases, and enzymes for aryl polyene, lactone and ribosomal peptide biosynthesis. Our in silico analysis indicated that the family Acetobacteraceae is a potential source of many undiscovered bacterial metabolites and deserves more detailed experimental exploration.

Topics: Acetobacteraceae; Biosynthetic Pathways; Multigene Family; Phylogeny

PubMed: 34761294
DOI: 10.1007/s10482-021-01676-7

Authors: Boris Magasanik

Topics: Acetobacter; Biochemistry; Enterobacter aerogenes; History, 20th Century; Microbiology; Mutation; United States

PubMed: 15840567
DOI: 10.1074/jbc.X500003200

Review

Authors: Gabrielle Alves Ribeiro da Silva, Simone Santos de Sousa Oliveira, Sara Fernandes Lima...

Gluconobacter oxydans is a well-known acetic acid bacterium that has long been applied in the biotechnological industry. Its extraordinary capacity to oxidize a variety of sugars, polyols, and alcohols into acids, aldehydes, and ketones is advantageous for the production of valuable compounds. Relevant G. oxydans industrial applications are in the manufacture of L-ascorbic acid (vitamin C), miglitol, gluconic acid and its derivatives, and dihydroxyacetone. Increasing efforts on improving these processes have been made in the last few years, especially by applying metabolic engineering. Thereby, a series of genes have been targeted to construct powerful recombinant strains to be used in optimized fermentation. Furthermore, low-cost feedstocks, mostly agro-industrial wastes or byproducts, have been investigated, to reduce processing costs and improve the sustainability of G. oxydans bioprocess. Nonetheless, further research is required mainly to make these raw materials feasible at the industrial scale. The current shortage of suitable genetic tools for metabolic engineering modifications in G. oxydans is another challenge to be overcome. This paper aims to give an overview of the most relevant industrial G. oxydans processes and the current strategies developed for their improvement.

Topics: Acetic Acid; Biotechnology; Fermentation; Gluconobacter oxydans; Metabolic Engineering

PubMed: 35688964
DOI: 10.1007/s11274-022-03310-8

Authors: Bryan P Brown, Jennifer J Wernegreen

BACKGROUND

Symbiotic associations between gut microbiota and their animal hosts shape the evolutionary trajectories of both partners. The genomic consequences of these relationships are significantly influenced by a variety of factors, including niche localization, interaction potential, and symbiont transmission mode. In eusocial insect hosts, socially transmitted gut microbiota may represent an intermediate point between free living or environmentally acquired bacteria and those with strict host association and maternal transmission.

RESULTS

We characterized the bacterial communities associated with an abundant ant species, Camponotus chromaiodes. While many bacteria had sporadic distributions, some taxa were abundant and persistent within and across ant colonies. Specially, two Acetobacteraceae operational taxonomic units (OTUs; referred to as AAB1 and AAB2) were abundant and widespread across host samples. Dissection experiments confirmed that AAB1 and AAB2 occur in C. chromaiodes gut tracts. We explored the distribution and evolution of these Acetobacteraceae OTUs in more depth. We found that Camponotus hosts representing different species and geographical regions possess close relatives of the Acetobacteraceae OTUs detected in C. chromaiodes. Phylogenetic analysis revealed that AAB1 and AAB2 join other ant associates in a monophyletic clade. This clade consists of Acetobacteraceae from three ant tribes, including a third, basal lineage associated with Attine ants. This ant-specific AAB clade exhibits a significant acceleration of substitution rates at the 16S rDNA gene and elevated AT content. Substitutions along 16S rRNA in AAB1 and AAB2 result in ~10 % reduction in the predicted rRNA stability.

CONCLUSIONS

Combined, these patterns in Camponotus-associated Acetobacteraceae resemble those found in cospeciating gut associates that are both socially and maternally transmitted. These associates may represent an intermediate point along an evolutionary trajectory manifest most extremely in symbionts with strict maternal transmission. Collectively, these results suggest that Acetobacteraceae may be a frequent and persistent gut associate in Camponotus species and perhaps other ant groups, and that its evolution is strongly impacted by this host association.

Topics: Acetobacteraceae; Animals; Ants; Base Sequence; Biodiversity; Biological Evolution; DNA, Bacterial; DNA, Ribosomal; Evolution, Molecular; Gastrointestinal Microbiome; Genes, Bacterial; Host Specificity; Microbial Consortia; Phylogeny; RNA, Ribosomal, 16S; Sequence Alignment; Sequence Analysis, DNA; Symbiosis

PubMed: 27400652
DOI: 10.1186/s12866-016-0721-8

Review

Authors: Elena Crotti, Aurora Rizzi, Bessem Chouaia...

Recent research in microbe-insect symbiosis has shown that acetic acid bacteria (AAB) establish symbiotic relationships with several insects of the orders Diptera, Hymenoptera, Hemiptera, and Homoptera, all relying on sugar-based diets, such as nectars, fruit sugars, or phloem sap. To date, the fruit flies Drosophila melanogaster and Bactrocera oleae, mosquitoes of the genera Anopheles and Aedes, the honey bee Apis mellifera, the leafhopper Scaphoideus titanus, and the mealybug Saccharicoccus sacchari have been found to be associated with the bacterial genera Acetobacter, Gluconacetobacter, Gluconobacter, Asaia, and Saccharibacter and the novel genus Commensalibacter. AAB establish symbiotic associations with the insect midgut, a niche characterized by the availability of diet-derived carbohydrates and oxygen and by an acidic pH, selective factors that support AAB growth. AAB have been shown to actively colonize different insect tissues and organs, such as the epithelia of male and female reproductive organs, the Malpighian tubules, and the salivary glands. This complex topology of the symbiosis indicates that AAB possess the keys for passing through body barriers, allowing them to migrate to different organs of the host. Recently, AAB involvement in the regulation of innate immune system homeostasis of Drosophila has been shown, indicating a functional role in host survival. All of these lines of evidence indicate that AAB can play different roles in insect biology, not being restricted to the feeding habit of the host. The close association of AAB and their insect hosts has been confirmed by the demonstration of multiple modes of transmission between individuals and to their progeny that include vertical and horizontal transmission routes, comprising a venereal one. Taken together, the data indicate that AAB represent novel secondary symbionts of insects.

Topics: Acetobacteraceae; Animals; Culicidae; Digestive System; Drosophila melanogaster; Female; Insecta; Male; Phylogeny; Symbiosis

PubMed: 20851977
DOI: 10.1128/AEM.01336-10

Authors: Ly Tu Phung, Haruthairat Kitwetcharoen, Nuttaporn Chamnipa...

Several raw materials have been used as partial supplements or entire replacements for the main ingredients of kombucha to improve the biological properties of the resulting kombucha beverage. This study used pineapple peels and cores (PPC), byproducts of pineapple processing, as alternative raw materials instead of sugar for kombucha production. Kombuchas were produced from fusions of black tea and PPC at different ratios, and their chemical profiles and biological properties, including antioxidant and antimicrobial activities, were determined and compared with the control kombucha without PPC supplementation. The results showed that PPC contained high amounts of beneficial substances, including sugars, polyphenols, organic acids, vitamins, and minerals. An analysis of the microbial community in a kombucha SCOBY (Symbiotic Cultures of Bacteria and Yeasts) using next-generation sequencing revealed that Acetobacter and Komagataeibacter were the most predominant acetic acid bacteria. Furthermore, Dekkera and Bacillus were also the prominent yeast and bacteria in the kombucha SCOBY. A comparative analysis was performed for kombucha products fermented using black tea and a fusion of black tea and PPC, and the results revealed that the kombucha made from the black tea and PPC infusion exhibited a higher total phenolic content and antioxidant activity than the control kombucha. The antimicrobial properties of the kombucha products made from black tea and the PPC infusion were also greater than those of the control. Several volatile compounds that contributed to the flavor, aroma, and beneficial health properties, such as esters, carboxylic acids, phenols, alcohols, aldehydes, and ketones, were detected in kombucha products made from a fusion of black tea and PPC. This study shows that PPC exhibits high potential as a supplement to the raw material infusion used with black tea for functional kombucha production.

Topics: Tea; Ananas; Beverages; Yeasts; Antioxidants; Camellia sinensis; Phenols; Anti-Infective Agents; Acetobacteraceae; Fermentation

PubMed: 37188725
DOI: 10.1038/s41598-023-34954-7

Authors: Julie M Laurent, Ankit Jain, Anton Kan...

Nature is home to a variety of microorganisms that create materials under environmentally friendly conditions. While this offers an attractive approach for sustainable manufacturing, the production of materials by native microorganisms is usually slow and synthetic biology tools to engineer faster microorganisms are only available when prior knowledge of genotype-phenotype links is available. Here, we utilize a high-throughput directed evolution platform to enhance the fitness of whole microorganisms under selection pressure and identify genetic pathways to enhance the material production capabilities of native species. Using as a model cellulose-producing microorganism, we show that our droplet-based microfluidic platform enables the directed evolution of these bacteria toward a small number of cellulose overproducers from an initial pool of 40,000 random mutants. Sequencing of the evolved strains reveals an unexpected link between the cellulose-forming ability of the bacteria and a gene encoding a protease complex responsible for protein turnover in the cell. The ability to enhance the fitness of microorganisms toward a specific phenotype and to unravel genotype-phenotype links makes this high-throughput directed evolution platform a promising tool for the development of new strains for the sustainable manufacturing of materials.

Topics: Cellulose; Directed Molecular Evolution; Acetobacteraceae; Phenotype; Mutation

PubMed: 39042685
DOI: 10.1073/pnas.2403585121