Spermidine regulates<i>Vibrio cholerae</i>biofilm formation via transport and signaling pathways

McGinnis, Marcus W.; Parker, Zachary M.; Walter, Nicholas E.; Rutkovsky, Alex; Cartaya-Marin, Claudia P.; Karatan, Ece

doi:10.1111/j.1574-6968.2009.01744.x

Cited by 83 publications

(124 citation statements)

References 28 publications

Supporting

Mentioning

113

Contrasting

Unclassified

Order By: Relevance

“…In uropathogenic E. coli, nitrosative stress has been shown to increase polyamine production, which was linked to RNS resistance (33), suggesting that such a mechanism might exist in V. cholerae, too. Polyamines have also been linked to biofilm production in V. cholerae (34). Furthermore, NO sensing has been shown to influence biofilm formation in other bacterial species through H-NOX domain proteins and cyclic-di-GMP production (35)(36)(37).…”

Section: Discussionmentioning

confidence: 99%

A Novel Protein Protects Bacterial Iron-Dependent Metabolism from Nitric Oxide

et al. 2013

View full text Add to dashboard Cite

Reactive nitrogen species (RNS), in particular nitric oxide (NO), are toxic to bacteria, and bacteria have mechanisms to allow growth despite this stress. Understanding how bacteria interact with NO is essential to understanding bacterial physiology in many habitats, including pathogenesis; however, many targets of NO and enzymes involved in NO resistance remain uncharacterized. We performed for the first time a metabolomic screen on NO-treated and -untreated bacteria to define broadly the effects of NO on bacterial physiology, as well as to identify the function of NnrS, a previously uncharacterized enzyme involved in defense against NO. We found many known and novel targets of NO. We also found that iron-sulfur cluster enzymes were preferentially inhibited in a strain lacking NnrS due to the formation of iron-NO complexes. We then demonstrated that NnrS is particularly important for resistance to nitrosative stress under anaerobic conditions. Our data thus reveal the breadth of the toxic effects of NO on metabolism and identify the function of an important enzyme in alleviating this stress. Vibrio cholerae causes cholera, a severe watery diarrhea responsible for millions of cases and thousands of deaths each year (Centers for Disease Control and Prevention [http://www.cdc .gov]). It is not, however, a member of the Enterobacteriaceae-its natural habitat is aquatic. It is thought that during most of its life cycle, when not infecting humans, V. cholerae resides in association with zooplankton, forming biofilms on the chitinous surfaces of crustaceans (1, 2). Thus, V. cholerae must display metabolic flexibility in order to thrive in these two different environments and respond to the different metabolic challenges therein.A commonly encountered metabolic stress for pathogenic and nonpathogenic bacteria is the presence of reactive nitrogen species (RNS), in particular the well-studied molecule nitric oxide (NO). NO is formed as a by-product of nitrogen metabolism for many bacteria as an intermediate in denitrification (3), as well as from dedicated nitric oxide synthases (NOSs) in both bacteria and eukaryotes (4, 5), and is present in micromolar concentrations in some bacterial biofilms (6). NO can also be formed by chemical decomposition of nitrite in acid environments, such as the human stomach (7). NO is also a prominent component of the mammalian innate immune system, part of a battery of reactive oxygen species (ROS) and RNS produced by phagocytes when they encounter bacteria (7).The mechanisms whereby NO inhibits bacterial growth are diverse, but one of the most important properties of NO is its ability to bind iron and form dinitrosyl iron complexes (DNICs) bound to iron-sulfur cluster proteins, inhibiting their function (8, 9). DNICs have also been shown to mediate the formation of nitrosothiols, another form of nitrosative stress that inhibits thiolcontaining proteins (10). Through this mechanism and others, NO has been shown to inhibit a few enzymes in vitro, including such central metabolic enzymes as ...

show abstract

Section: Discussionmentioning

confidence: 99%

A Novel Protein Protects Bacterial Iron-Dependent Metabolism from Nitric Oxide

et al. 2013

View full text Add to dashboard Cite

show abstract

“…Exogenous spermidine has the opposite effect, inhibiting biofilm formation, and this also requires NspS (32). These responses are mediated through a transmembrane protein called MbaA, originally identified as a repressor of biofilm formation (33).…”

Section: Figmentioning

confidence: 99%

Spermidine Inversely Influences Surface Interactions and Planktonic Growth in Agrobacterium tumefaciens

et al. 2016

View full text Add to dashboard Cite

In bacteria, the functions of polyamines, small linear polycations, are poorly defined, but these metabolites can influence biofilm formation in several systems. Transposon insertions in an ornithine decarboxylase (odc) gene in Agrobacterium tumefaciens, predicted to direct synthesis of the polyamine putrescine from ornithine, resulted in elevated cellulose. Null mutants for odc grew somewhat slowly in a polyamine-free medium but exhibited increased biofilm formation that was dependent on cellulose production. Spermidine is an essential metabolite in A. tumefaciens and is synthesized from putrescine in A. tumefaciens via the stepwise actions of carboxyspermidine dehydrogenase (CASDH) and carboxyspermidine decarboxylase (CASDC). Exogenous addition of either putrescine or spermidine to the odc mutant returned biofilm formation to wild-type levels. Low levels of exogenous spermidine restored growth to CASDH and CASDC mutants, facilitating weak biofilm formation, but this was dampened with increasing concentrations. Norspermidine rescued growth for the odc, CASDH, and CASDC mutants but did not significantly affect their biofilm phenotypes, whereas in the wild type, it stimulated biofilm formation and depressed spermidine levels. The odc mutant produced elevated levels of cyclic diguanylate monophosphate (c-di-GMP), exogenous polyamines modulated these levels, and expression of a c-di-GMP phosphodiesterase reversed the enhanced biofilm formation. Prior work revealed accumulation of the precursors putrescine and carboxyspermidine in the CASDH and CASDC mutants, respectively, but unexpectedly, both mutants accumulated homospermidine; here, we show that this requires a homospermidine synthase (hss) homologue. IMPORTANCEPolyamines are small, positively charged metabolites that are nearly ubiquitous in cellular life. They are often essential in eukaryotes and more variably in bacteria. Polyamines have been reported to influence the surface-attached biofilm formation of several bacteria. In Agrobacterium tumefaciens, mutants with diminished levels of the polyamine spermidine are stimulated for biofilm formation, and exogenous provision of spermidine decreases biofilm formation. Spermidine is also essential for A. tumefaciens growth, but the related polyamine norspermidine exogenously rescues growth and does not diminish biofilm formation, revealing that the growth requirement and biofilm control are separable. Polyamine control of biofilm formation appears to function via effects on the cellular second messenger cyclic diguanylate monophosphate, regulating the transition from a freeliving to a surface-attached lifestyle.

show abstract

“…Surface-associated bacteria usually harbor more c-di-GMP regulators than free-living bacteria, presumably as an adaptive strategy (120). O 2 , H 2 O 2 , NO, redox potential, light, sucrose, amino acids, polyamines (such as norspermidine and spermidine), Zn 2ϩ , bile acids, bicarbonate, indole, QS autoinducers, cis-2-dodecenoic acid and cis-11-methyl-dodecenoic acid (unsaturated fatty acids that serve as bacterial diffusible signal factors), and nutritional conditions that cause starvation (or depletion of a specific carbon source such as glucose or glycerol) have been identified as environmental cues that induce the bacterial response via altering the intracellular c-di-GMP concentration (480,(492)(493)(494)(495)(496)(497)(498)(499)(500)(501)(502)(503)(504)(505)(506)(507)(508). However, the vast majority of the environmental signals that modulate the activity of the DGCs and PDEs remain unidentified.…”

Section: Centralized Regulation By Second Messengersmentioning

confidence: 99%

Microbial Surface Colonization and Biofilm Development in Marine Environments

Dang

Lovell

2016

Microbiol Mol Biol Rev

870

636

View full text Add to dashboard Cite

SUMMARYBiotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.

show abstract

Spermidine regulatesVibrio choleraebiofilm formation via transport and signaling pathways

Cited by 83 publications

References 28 publications

A Novel Protein Protects Bacterial Iron-Dependent Metabolism from Nitric Oxide

A Novel Protein Protects Bacterial Iron-Dependent Metabolism from Nitric Oxide

Spermidine Inversely Influences Surface Interactions and Planktonic Growth in Agrobacterium tumefaciens

Microbial Surface Colonization and Biofilm Development in Marine Environments

Contact Info

Product

Resources

About