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• W4295079795 abstract "The biofilm lifestyle is the prevalent prokaryotic mode of life in numerous habitats and represents a niche colonization mechanism subjected to a swift regulation by external and internal cues. Respiration is a ubiquitous form of energy acquisition. Metabolic resources driving competition for a niche include electron acceptors used for respiration.Growing evidence from diverse bacterial species suggests intimate links between respiration and biofilm turnover. This ubiquity could imply a potential universal nature of this phenomenon across the kingdom Bacteria. Recent evidence shows that respiration-induced promotion or dispersal of biofilms can be strain-specific even if the same respiration pathways are conserved, functional, and expressed by the individual strains.Respiration-induced biofilm formation might aid the occupation of distinct niches by redox-specialized species or strains within the same species, potentially contributing to bacterial speciation, and opening up for a palette of yet virtually unexplored social microbial interactions.Understanding respiration-induced biofilm formation mechanisms will provide novel insights into microbial ecology, ranging from bacterial community structure and composition in stratified environments to host colonization by bacterial pathogens or commensals. Targeting or engineering such mechanisms may enable an array of applications in biomedicine or biotechnology and lay the ground to new approaches for fighting antibiotic resistance. Depending on their physiology and metabolism, bacteria can carry out diverse redox processes for energy acquisition, which facilitates adaptation to environmental or host-associated niches. Of these processes, respiration, using oxygen or alternative terminal electron acceptors, is energetically the most favorable in heterotrophic bacteria. The biofilm lifestyle, a coordinated multicellular behavior, is ubiquitous in bacteria and is regulated by a variety of intrinsic and extrinsic cues. Respiration of distinct electron acceptors has been shown to induce biofilm formation or dispersal. The notion of biofilm formation regulation by electron acceptor availability and respiration has often been considered species-specific. However, recent evidence suggests that this phenomenon can be strain-specific, even in strains sharing the same functional respiratory pathways, thereby implying subtle regulatory mechanisms. On this basis, I argue that induction of biofilm formation by sensing and respiration of electron acceptors might direct subgroups of redox-specialized strains to occupy certain niches. A palette of respiration and electron-transfer-mediated microbial social interactions within biofilms may broaden ecological opportunities. The strain specificity of this phenomenon represents an important opportunity to identify key molecular mechanisms and their ecophysiological significance, which in turn may lay the ground for applications in areas ranging from biotechnology to the prevention of antimicrobial resistance. Depending on their physiology and metabolism, bacteria can carry out diverse redox processes for energy acquisition, which facilitates adaptation to environmental or host-associated niches. Of these processes, respiration, using oxygen or alternative terminal electron acceptors, is energetically the most favorable in heterotrophic bacteria. The biofilm lifestyle, a coordinated multicellular behavior, is ubiquitous in bacteria and is regulated by a variety of intrinsic and extrinsic cues. Respiration of distinct electron acceptors has been shown to induce biofilm formation or dispersal. The notion of biofilm formation regulation by electron acceptor availability and respiration has often been considered species-specific. However, recent evidence suggests that this phenomenon can be strain-specific, even in strains sharing the same functional respiratory pathways, thereby implying subtle regulatory mechanisms. On this basis, I argue that induction of biofilm formation by sensing and respiration of electron acceptors might direct subgroups of redox-specialized strains to occupy certain niches. A palette of respiration and electron-transfer-mediated microbial social interactions within biofilms may broaden ecological opportunities. The strain specificity of this phenomenon represents an important opportunity to identify key molecular mechanisms and their ecophysiological significance, which in turn may lay the ground for applications in areas ranging from biotechnology to the prevention of antimicrobial resistance. A hallmark of life is energy conservation through redox reactions. This paradigm is the essence of bacterial energy metabolism (see Glossary) and cellular respiration (Box 1). Facultative anaerobic bacteria employ molecular oxygen or alternative electron acceptors (AEAs) as the terminal sink for the electrons shuttled across the electron transport chain. This physiological versatility allows facultative anaerobes to thrive in oxygen-rich as well as oxygen-depleted environments. A primary strategy to occupy an ecological niche is through the formation of a biofilm. Benefits of biofilm formation include protection against physical and chemical stressors, environmental persistence, and a more efficient acquisition and use of nutrients. These collective advantages promote the ubiquity and resilience of this lifestyle in nature. Indeed, recent estimates highlight the biofilm lifestyle as the prevalent prokaryotic mode of life in numerous ecological niches [1.Flemming H.C. Wuertz S. Bacteria and archaea on Earth and their abundance in biofilms.Nat. Rev. Microbiol. 2019; 17: 247-260Crossref PubMed Scopus (701) Google Scholar]. Biofilms can occur in environments with variable levels of oxygen or AEAs. At the same time, stratified multispecies communities within biofilms are exposed to intrinsic oxygen and nutrient gradients that generate distinct local microenvironments, thereby imposing energy acquisition to occur through a certain set of reactions.Box 1Energy metabolismEnergy metabolism is a hallmark of cellular life. Generation of ATP occurs most efficiently through the establishment of a redox potential gradient between an electron donor and acceptor (see Figure 2A in the main text). The most efficient means for energy generation are photosynthesis and either aerobic or anaerobic respiration. Bacterial respiratory chains are remarkably flexible and can employ diverse combinations of electron donors and acceptors, even simultaneously. In the absence of oxygen or suitable AEAs, fermentation generates low ATP yields using an endogenous electron acceptor, most frequently pyruvate, through substrate-level phosphorylation. Fermentation waste-products include carbon dioxide, hydrogen gas, and a diversity of organic compounds, such as ethanol or carboxylic acids, with industrial and environmental significance.Respiration generates ATP through membrane-associated ATP synthases. Recycling of reduction equivalents creates energy through electron transport at the (inner) membrane, ultimately building up a proton-motive force required for ATP synthesis. From an energetic standpoint, aerobic respiration, which uses oxygen as terminal electron acceptor, is the most efficient mode of ATP generation. Facultative and obligate anaerobes employ anaerobic respiration using inorganic compounds (e.g., NO3–, Fe3+, SO42–) or organic compounds [e.g., trimethylamine-N-oxide (TMAO), dimethylsulfoxide (DMSO)] as final electron acceptors. Anaerobic respiration has a wide impact on the global nitrogen and sulfur cycles. Denitrification, the reduction of inorganic nitrate, results in the production of molecular nitrogen, a gas that represents 78% of the atmosphere of planet Earth. The biogeochemical cycle of sulfur includes reduction of inorganic sulfate and sulfur intermediates to H2S, and ultimately to elemental sulfur. Hydrogen sulfide feeds anoxygenic photosynthesis by certain groups of phototrophs, such as green sulfur bacteria.Organic electron acceptors of broad ecological relevance are molecules such as TMAO and DMSO. TMAO is an osmolyte of marine animals. Trimethylamine, the product of TMAO reduction, constitutes an important seafood spoilage metabolite. DMSO is generated by bacterial and photochemical oxidation of dimethyl sulfide, or secreted by organisms such as algae and phytoplankton. In the atmosphere, DMSO molecules act as cloud condensation nuclei, leading to an increase in albedo, a phenomenon with major repercussion for global climate.Biogeochemical cycles are often intertwined. For example, metal ions like Fe(III) or Mn(IV) also play significant biological and geochemical roles, and their natural cycles overlap closely with those of sulfur and nitrogen. Energy metabolism is a hallmark of cellular life. Generation of ATP occurs most efficiently through the establishment of a redox potential gradient between an electron donor and acceptor (see Figure 2A in the main text). The most efficient means for energy generation are photosynthesis and either aerobic or anaerobic respiration. Bacterial respiratory chains are remarkably flexible and can employ diverse combinations of electron donors and acceptors, even simultaneously. In the absence of oxygen or suitable AEAs, fermentation generates low ATP yields using an endogenous electron acceptor, most frequently pyruvate, through substrate-level phosphorylation. Fermentation waste-products include carbon dioxide, hydrogen gas, and a diversity of organic compounds, such as ethanol or carboxylic acids, with industrial and environmental significance. Respiration generates ATP through membrane-associated ATP synthases. Recycling of reduction equivalents creates energy through electron transport at the (inner) membrane, ultimately building up a proton-motive force required for ATP synthesis. From an energetic standpoint, aerobic respiration, which uses oxygen as terminal electron acceptor, is the most efficient mode of ATP generation. Facultative and obligate anaerobes employ anaerobic respiration using inorganic compounds (e.g., NO3–, Fe3+, SO42–) or organic compounds [e.g., trimethylamine-N-oxide (TMAO), dimethylsulfoxide (DMSO)] as final electron acceptors. Anaerobic respiration has a wide impact on the global nitrogen and sulfur cycles. Denitrification, the reduction of inorganic nitrate, results in the production of molecular nitrogen, a gas that represents 78% of the atmosphere of planet Earth. The biogeochemical cycle of sulfur includes reduction of inorganic sulfate and sulfur intermediates to H2S, and ultimately to elemental sulfur. Hydrogen sulfide feeds anoxygenic photosynthesis by certain groups of phototrophs, such as green sulfur bacteria. Organic electron acceptors of broad ecological relevance are molecules such as TMAO and DMSO. TMAO is an osmolyte of marine animals. Trimethylamine, the product of TMAO reduction, constitutes an important seafood spoilage metabolite. DMSO is generated by bacterial and photochemical oxidation of dimethyl sulfide, or secreted by organisms such as algae and phytoplankton. In the atmosphere, DMSO molecules act as cloud condensation nuclei, leading to an increase in albedo, a phenomenon with major repercussion for global climate. Biogeochemical cycles are often intertwined. For example, metal ions like Fe(III) or Mn(IV) also play significant biological and geochemical roles, and their natural cycles overlap closely with those of sulfur and nitrogen. Two limiting resources drive microbial competition for a niche, namely, space, which provides the physical environment and mechanical support, and nutrients, which are essential for energy acquisition [2.Ghoul M. Mitri S. The ecology and evolution of microbial competition.Trends Microbiol. 2016; 24: 833-845Abstract Full Text Full Text PDF PubMed Scopus (388) Google Scholar]. Thus, in essence, microbial niche occupation involves gaining control over the metabolic resources available at a certain habitat, which include electron acceptors whose utilization may provide a fitness advantage. Bacteria employ a plethora of strategies for niche occupation, largely marked by a constant warfare with other microbes [3.Elias S. Banin E. Multi-species biofilms: living with friendly neighbors.FEMS Microbiol. Rev. 2012; 36: 990-1004Crossref PubMed Scopus (486) Google Scholar,4.Hibbing M.E. et al.Bacterial competition: surviving and thriving in the microbial jungle.Nat. Rev. Microbiol. 2010; 8: 15-25Crossref PubMed Scopus (1610) Google Scholar]. In terms of lifestyle, the decision for the individual bacterial cell is reduced to essentially two possibilities (Figure 1A ): either planktonic (free-living) or sessile (biofilm-associated). In this opinion article I summarize data that suggest respiration to be an active, ubiquitous driver for biofilm formation and niche occupation in bacteria (Box 2). I provide evidence showing that biofilm formation, or shifts in biofilm amount, are deeply intertwined with respiration of distinct electron acceptors, and that these links can be species or strain-specific. That is, respiration can induce biofilm formation or dispersal, a process that I refer to as ‘respiration-induced biofilm formation’ (RIBF) or ‘respiration-induced biofilm dispersal’ (RIBD), respectively. While examples of both phenomena are presented, the main focus of this opinion piece is on RIBF because of its implication in surface colonization.Box 2Is RIBF universal?The iron–sulfur world hypothesis by Günter Wächtershäuser [21.Wächtershäuser G. Before enzymes and templates: theory of surface metabolism.Microbiol. Rev. 1988; 52: 452-484Crossref PubMed Google Scholar] already postulated the first cells – and the first energy metabolism – to have evolved from ancestral ‘surface metabolists’, primeval acellular organisms anionically bound to mineral surfaces containing iron, nickel, and sulfur, which catalyzed the synthesis of the precursor organic compounds needed for life. Fe-S clusters mediate electron transfer reactions. Fe-S cluster-containing proteins are universal in all branches of life and participate in diverse cellular processes, including the electron transport chain and respiration. Irrespective of how the first cells appeared and evolved, it is clear that a surface-associated, biofilm mode of life is deeply rooted into the biology of bacteria, and that this lifestyle has tight links with energy metabolism. Indeed, RIBF extends phylogenetically and seems to be widespread in bacteria. In colony biofilms of the gammaproteobacterial species E. coli and Salmonella, the so-called rdar (red, dry, and rough) morphotype on Congo Red-supplemented agar is characterized by the production of biofilm extracellular matrix components, primarily the exopolysaccharide cellulose and fibril-forming amyloid curli fimbriae. Strains of different E. coli pathotypes, including uropathogenic [22.Martín-Rodríguez A.J. et al.Nitrate metabolism modulates biosynthesis of biofilm components in uropathogenic Escherichia coli and acts as a fitness factor during experimental urinary tract infection.Front. Microbiol. 2020; 11: 26Crossref PubMed Scopus (18) Google Scholar] and enterotoxigenic strains (Martín-Rodríguez et al., unpublished), exhibit distinct colony biofilm morphotypes on nitrate-supplemented agar compared with nitrate-free medium. Thereby, certain strains downregulate rdar biofilm formation upon nitrate addition whereas a subset of strains exhibit exacerbated rdar morphotypes. The alteration in colony morphotypes is respiration-mediated [22.Martín-Rodríguez A.J. et al.Nitrate metabolism modulates biosynthesis of biofilm components in uropathogenic Escherichia coli and acts as a fitness factor during experimental urinary tract infection.Front. Microbiol. 2020; 11: 26Crossref PubMed Scopus (18) Google Scholar] and likely represents alternative lifestyle adaptation mechanisms to electron acceptor abundance or electron acceptor-induced stress. Research with Pseudomonas aeruginosa PA14 colony biofilms supports this notion [23.Dietrich L.E.P. et al.Bacterial community morphogenesis is intimately linked to the intracellular redox state.J. Bacteriol. 2013; 195: 1371-1380Crossref PubMed Scopus (203) Google Scholar,24.Madsen J.S. et al.Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models.Appl. Environ. Microbiol. 2015; 81: 8414-8426Crossref PubMed Scopus (49) Google Scholar]. P. aeruginosa offers indeed interesting insights into the intertwined metabolic links between respiration, redox homeostasis, and biofilm morphogenesis. In P. aeruginosa PA14, an orphan cbb3-type cytochrome c oxidase has been shown to support cell survival within biofilms via reduction of oxygen and the electron shuttle phenazine [25.Jo J. et al.An orphan cbb3-type cytochrome oxidase subunit supports Pseudomonas aeruginosa biofilm growth and virulence.Elife. 2017; 6e30205Crossref Scopus (50) Google Scholar]. Phenazines in turn have been shown to modulate PA14 intracellular c-di-GMP pools via the PAS-domain-containing c-di-GMP phosphodiesterase RmcA [26.Okegbe C. et al.Electron-shuttling antibiotics structure bacterial communities by modulating cellular levels of c-di-GMP.Proc. Natl. Acad. Sci. U. S. A. 2017; 114: E5236-E5245Crossref PubMed Scopus (60) Google Scholar], thereby regulating the biosynthesis of the biofilm exopolysaccharide Pel. Biofilms are stratified communities in which cells have different accessibility to oxygen and AEAs depending on their location. Such a stratification leads to the existence of bacterial subpopulations with distinct gene expression programs. In biofilms of the uropathogenic E. coli (UPEC) strain UTI89, production of adhesive type 1 fimbriae is positively regulated by oxygen, and consequently these appendages are expressed by air-exposed cells [27.Floyd K.A. et al.Adhesive fiber stratification in uropathogenic Escherichia coli biofilms unveils oxygen-mediated control of type 1 pili.PLoS Pathog. 2015; 11e1004697Crossref PubMed Scopus (60) Google Scholar]. Within colony biofilms, subpopulations of UTI89 cells express distinct levels of cytochrome bd, a proton-motive-force-generating terminal oxidase that positively contributes to biosynthesis of biofilm extracellular polymeric substances (EPSs) and colonization of organ niches during urinary tract infection [28.Beebout C.J. et al.Respiratory heterogeneity shapes biofilm formation and host colonization in uropathogenic Escherichia coli.mBio. 2019; 10e02400–18Crossref PubMed Scopus (48) Google Scholar].Respiration control of a multicellular, biofilm-associated lifestyle has also been documented beyond Gammaproteobacteria. In the Gram-negative, facultative anaerobic betaproteobacterium Neisseria gonorrhoeae, an obligate human pathogen and causative agent of gonorrhea, respiration via the truncated AniA–NorB denitrification pathway was shown to be required for biofilm establishment [29.Potter A.J. et al.Thioredoxin reductase is essential for protection of Neisseria gonorrhoeae against killing by nitric oxide and for bacterial growth during interaction with cervical epithelial cells.J. Infect. Dis. 2009; 199: 227-235Crossref PubMed Scopus (44) Google Scholar]. In the Gram-positive-dominated phylum Firmicutes, respiration-mediated biofilm regulation has been reported for the species Bacillus subtilis [30.Kolodkin-Gal I. et al.Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane-embedded histidine kinase.Genes Dev. 2013; 27: 887-899Crossref PubMed Scopus (104) Google Scholar,31.Qin Y. et al.Heterogeneity in respiratory electron transfer and adaptive iron utilization in a bacterial biofilm.Nat. Commun. 2019; 10: 3702Crossref PubMed Scopus (36) Google Scholar] and Staphylococcus aureus [32.Mashruwala A.A. et al.Impaired respiration elicits SrrAB-dependent programmed cell lysis and biofilm formation in Staphylococcus aureus.Elife. 2017; 6e23845Crossref PubMed Scopus (78) Google Scholar,33.Mashruwala A.A. et al.SaeRS is responsive to cellular respiratory status and regulates fermentative biofilm formation in Staphylococcus aureus.Infect. Immun. 2017; 85e00157–17Crossref Scopus (35) Google Scholar], thereby showcasing the potential universality of this phenomenon. In most cases, though, strain-specificity of respiration-mediated biofilm formation has not been addressed and therefore the responses of model strains are often assumed to be representative of the entire species. The iron–sulfur world hypothesis by Günter Wächtershäuser [21.Wächtershäuser G. Before enzymes and templates: theory of surface metabolism.Microbiol. Rev. 1988; 52: 452-484Crossref PubMed Google Scholar] already postulated the first cells – and the first energy metabolism – to have evolved from ancestral ‘surface metabolists’, primeval acellular organisms anionically bound to mineral surfaces containing iron, nickel, and sulfur, which catalyzed the synthesis of the precursor organic compounds needed for life. Fe-S clusters mediate electron transfer reactions. Fe-S cluster-containing proteins are universal in all branches of life and participate in diverse cellular processes, including the electron transport chain and respiration. Irrespective of how the first cells appeared and evolved, it is clear that a surface-associated, biofilm mode of life is deeply rooted into the biology of bacteria, and that this lifestyle has tight links with energy metabolism. Indeed, RIBF extends phylogenetically and seems to be widespread in bacteria. In colony biofilms of the gammaproteobacterial species E. coli and Salmonella, the so-called rdar (red, dry, and rough) morphotype on Congo Red-supplemented agar is characterized by the production of biofilm extracellular matrix components, primarily the exopolysaccharide cellulose and fibril-forming amyloid curli fimbriae. Strains of different E. coli pathotypes, including uropathogenic [22.Martín-Rodríguez A.J. et al.Nitrate metabolism modulates biosynthesis of biofilm components in uropathogenic Escherichia coli and acts as a fitness factor during experimental urinary tract infection.Front. Microbiol. 2020; 11: 26Crossref PubMed Scopus (18) Google Scholar] and enterotoxigenic strains (Martín-Rodríguez et al., unpublished), exhibit distinct colony biofilm morphotypes on nitrate-supplemented agar compared with nitrate-free medium. Thereby, certain strains downregulate rdar biofilm formation upon nitrate addition whereas a subset of strains exhibit exacerbated rdar morphotypes. The alteration in colony morphotypes is respiration-mediated [22.Martín-Rodríguez A.J. et al.Nitrate metabolism modulates biosynthesis of biofilm components in uropathogenic Escherichia coli and acts as a fitness factor during experimental urinary tract infection.Front. Microbiol. 2020; 11: 26Crossref PubMed Scopus (18) Google Scholar] and likely represents alternative lifestyle adaptation mechanisms to electron acceptor abundance or electron acceptor-induced stress. Research with Pseudomonas aeruginosa PA14 colony biofilms supports this notion [23.Dietrich L.E.P. et al.Bacterial community morphogenesis is intimately linked to the intracellular redox state.J. Bacteriol. 2013; 195: 1371-1380Crossref PubMed Scopus (203) Google Scholar,24.Madsen J.S. et al.Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models.Appl. Environ. Microbiol. 2015; 81: 8414-8426Crossref PubMed Scopus (49) Google Scholar]. P. aeruginosa offers indeed interesting insights into the intertwined metabolic links between respiration, redox homeostasis, and biofilm morphogenesis. In P. aeruginosa PA14, an orphan cbb3-type cytochrome c oxidase has been shown to support cell survival within biofilms via reduction of oxygen and the electron shuttle phenazine [25.Jo J. et al.An orphan cbb3-type cytochrome oxidase subunit supports Pseudomonas aeruginosa biofilm growth and virulence.Elife. 2017; 6e30205Crossref Scopus (50) Google Scholar]. Phenazines in turn have been shown to modulate PA14 intracellular c-di-GMP pools via the PAS-domain-containing c-di-GMP phosphodiesterase RmcA [26.Okegbe C. et al.Electron-shuttling antibiotics structure bacterial communities by modulating cellular levels of c-di-GMP.Proc. Natl. Acad. Sci. U. S. A. 2017; 114: E5236-E5245Crossref PubMed Scopus (60) Google Scholar], thereby regulating the biosynthesis of the biofilm exopolysaccharide Pel. Biofilms are stratified communities in which cells have different accessibility to oxygen and AEAs depending on their location. Such a stratification leads to the existence of bacterial subpopulations with distinct gene expression programs. In biofilms of the uropathogenic E. coli (UPEC) strain UTI89, production of adhesive type 1 fimbriae is positively regulated by oxygen, and consequently these appendages are expressed by air-exposed cells [27.Floyd K.A. et al.Adhesive fiber stratification in uropathogenic Escherichia coli biofilms unveils oxygen-mediated control of type 1 pili.PLoS Pathog. 2015; 11e1004697Crossref PubMed Scopus (60) Google Scholar]. Within colony biofilms, subpopulations of UTI89 cells express distinct levels of cytochrome bd, a proton-motive-force-generating terminal oxidase that positively contributes to biosynthesis of biofilm extracellular polymeric substances (EPSs) and colonization of organ niches during urinary tract infection [28.Beebout C.J. et al.Respiratory heterogeneity shapes biofilm formation and host colonization in uropathogenic Escherichia coli.mBio. 2019; 10e02400–18Crossref PubMed Scopus (48) Google Scholar]. Respiration control of a multicellular, biofilm-associated lifestyle has also been documented beyond Gammaproteobacteria. In the Gram-negative, facultative anaerobic betaproteobacterium Neisseria gonorrhoeae, an obligate human pathogen and causative agent of gonorrhea, respiration via the truncated AniA–NorB denitrification pathway was shown to be required for biofilm establishment [29.Potter A.J. et al.Thioredoxin reductase is essential for protection of Neisseria gonorrhoeae against killing by nitric oxide and for bacterial growth during interaction with cervical epithelial cells.J. Infect. Dis. 2009; 199: 227-235Crossref PubMed Scopus (44) Google Scholar]. In the Gram-positive-dominated phylum Firmicutes, respiration-mediated biofilm regulation has been reported for the species Bacillus subtilis [30.Kolodkin-Gal I. et al.Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane-embedded histidine kinase.Genes Dev. 2013; 27: 887-899Crossref PubMed Scopus (104) Google Scholar,31.Qin Y. et al.Heterogeneity in respiratory electron transfer and adaptive iron utilization in a bacterial biofilm.Nat. Commun. 2019; 10: 3702Crossref PubMed Scopus (36) Google Scholar] and Staphylococcus aureus [32.Mashruwala A.A. et al.Impaired respiration elicits SrrAB-dependent programmed cell lysis and biofilm formation in Staphylococcus aureus.Elife. 2017; 6e23845Crossref PubMed Scopus (78) Google Scholar,33.Mashruwala A.A. et al.SaeRS is responsive to cellular respiratory status and regulates fermentative biofilm formation in Staphylococcus aureus.Infect. Immun. 2017; 85e00157–17Crossref Scopus (35) Google Scholar], thereby showcasing the potential universality of this phenomenon. In most cases, though, strain-specificity of respiration-mediated biofilm formation has not been addressed and therefore the responses of model strains are often assumed to be representative of the entire species. Importantly, the strain-specificity of RIBF and RIBD strongly points to the existence of subgroups of strains within the same species that I postulate might be directed to occupy rather specific niches, aided by subtle regulatory mechanisms that go beyond the mere metabolic capacity to use a given energy resource and therefore energy acquisition per se. Thus, as electron acceptor-specific biofilm formation can occur in strains that otherwise share the same functional respiratory pathways, I discuss mechanisms and additional physiological, genomic, and gene-expression characteristics that may aid niche colonization by specialized strains, potentially contributing to bacterial speciation. Finally, I present insight on how RIBF can become a target for novel therapeutic agents, or for the controlled modulation of beneficial biofilms in diverse contexts. A strategy to outcompete less-fit counterparts involves the use of the available resources to support planktonic population expansion (Figure 1A). For example, Salmonella enterica serovar Typhimurium (S. Typhimurium) strain IR715 elicits intestinal inflammation, thereby inducing an oxidative burst that results in tetrathionate production from gut sulfur pools. Locally produced tetrathionate acts as a terminal electron acceptor that boosts pathogen growth and facilitates its dissemination [5.Winter S.E. et al.Gut inflammation provides a respiratory electron acceptor for Salmonella.Nature. 2010; 467: 426-429Crossref PubMed Scopus (872) Google Scholar]. The generation of reactive oxygen and nitrogen species during colonic inflammation results in local production of nitrate, an AEA that triggers S. Typhimurium IR715 anaerobic metabolism and induces the expression of the prpBCDE operon enabling propionate breakdown [6.Shelton C.D. et al.Salmonella enterica serovar Typhimurium uses anaerobic respiration to overcome propionate-mediated colonization resistance.Cell Rep. 2022; 38110180Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar]. Propionate is a short-chain fatty acid that causes toxicity and growth arrest in S. Typhimurium, so its degradation supports population expansion by the pathogen. Remarkably, parts of the prpBCDE operon are non-functional in extraintestinal Salmonella serovars, a signature of metabol" @default.
• W4295079795 created "2022-09-10" @default.
• W4295079795 creator A5041563935 @default.
• W4295079795 date "2023-02-01" @default.
• W4295079795 modified "2023-09-30" @default.
• W4295079795 title "Respiration-induced biofilm formation as a driver for bacterial niche colonization" @default.
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