Elucidation of the <scp><i>B</i></scp><i>urkholderia cenocepacia</i> hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid‐producing bacteria

Schmerk, Crystal L.; Welander, Paula V.; Hamad, Mohamad A.; Bain, Katie L.; Bernards, Mark A.; Summons, Roger E.; Valvano, Miguel A.

doi:10.1111/1462-2920.12509

Cited by 62 publications

(80 citation statements)

References 68 publications

(115 reference statements)

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“…As mentioned above, the squalene-hopene cyclase is also required, but it is unclear if any additional characteristics of Shc or the cellular environment in tetrahymanol-producing bacteria are necessary. To test this, we expressed M. alcaliphilum ths in two hopanoid-producing strains that typically do not synthesize tetrahymanol, the γ-Proteobacterium Methylococcus capsulatus Bath (36) and the β-Proteobacterium Burkholderia phytofirmans PsJN (37,38). Both ths + strains produced tetrahymanol (Fig.…”

Section: Resultsmentioning

confidence: 99%

A distinct pathway for tetrahymanol synthesis in bacteria

Banta

Wei

Welander

2015

Proc. Natl. Acad. Sci. U.S.A.

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Tetrahymanol is a polycyclic triterpenoid lipid first discovered in the ciliate Tetrahymena pyriformis whose potential diagenetic product, gammacerane, is often used as a biomarker for water column stratification in ancient ecosystems. Bacteria are also a potential source of tetrahymanol, but neither the distribution of this lipid in extant bacteria nor the significance of bacterial tetrahymanol synthesis for interpreting gammacerane biosignatures is known. Here we couple comparative genomics with genetic and lipid analyses to link a protein of unknown function to tetrahymanol synthesis in bacteria. This tetrahymanol synthase (Ths) is found in a variety of bacterial genomes, including aerobic methanotrophs, nitrite-oxidizers, and sulfate-reducers, and in a subset of aquatic and terrestrial metagenomes. Thus, the potential to produce tetrahymanol is more widespread in the bacterial domain than previously thought. However, Ths is not encoded in any eukaryotic genomes, nor is it homologous to eukaryotic squalene-tetrahymanol cyclase, which catalyzes the cyclization of squalene directly to tetrahymanol. Rather, heterologous expression studies suggest that bacteria couple the cyclization of squalene to a hopene molecule by squalene-hopene cyclase with a subsequent Ths-dependent ring expansion to form tetrahymanol. Thus, bacteria and eukaryotes have evolved distinct biochemical mechanisms for producing tetrahymanol.gammacerane | tetrahymanol | biomarkers | methanotrophs | sterols

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Section: Resultsmentioning

confidence: 99%

A distinct pathway for tetrahymanol synthesis in bacteria

Banta

Wei

Welander

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Hopanoids play an important role in bacterial interaction, conferring tolerance and improving the adaptation of bacteria in different environments 63, 64, 65. In fungi, the compounds differentially regulated in an interaction are often bioactive secondary metabolites, such as diketopiperazines, trichothecenes, atranones, and polyketides 14, 17.…”

Section: Secondary Metabolismmentioning

confidence: 99%

“…They are responsible for stabilization of the membrane and regulates its fluidity and permeability 79 . Experiments that knockout biosynthesis genes such as hnp F (squalene hopene cyclase-shc) gene shows that the absence of hopanoids does not influence bacterial growth,79, 80 but affects tolerance to several stress conditions, such as extremely acidic environments 81 ; toxic compounds as dichloromethane (DCM) 82 ; it also affects the resistance to antibiotics 64 and antimicrobial lipopeptide 63 ; playing a role in multidrug transport 83 and bacterial motility 84 …”

Section: Secondary Metabolismmentioning

confidence: 99%

“…Hopanoids act increasing bacteria tolerance to adverse environments, conferring resistance to stress conditions including extreme pH and temperature, and exposure to detergents and antibiotics 63, 64. In this way, hopanoids may be involved in bacteria–plant interaction, being responsible for adaptation of bacteria in aerobic micro-environment and low pH culture medium 65 ; as well as involved in nitrogen metabolism in Frankia sp 85 .…”

Section: Secondary Metabolismmentioning

confidence: 99%

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Microbial interactions: ecology in a molecular perspective

Braga

Dourado

Araújo

2016

Brazilian Journal of Microbiology

283

145

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The microorganism–microorganism or microorganism–host interactions are the key strategy to colonize and establish in a variety of different environments. These interactions involve all ecological aspects, including physiochemical changes, metabolite exchange, metabolite conversion, signaling, chemotaxis and genetic exchange resulting in genotype selection. In addition, the establishment in the environment depends on the species diversity, since high functional redundancy in the microbial community increases the competitive ability of the community, decreasing the possibility of an invader to establish in this environment. Therefore, these associations are the result of a co-evolution process that leads to the adaptation and specialization, allowing the occupation of different niches, by reducing biotic and abiotic stress or exchanging growth factors and signaling. Microbial interactions occur by the transference of molecular and genetic information, and many mechanisms can be involved in this exchange, such as secondary metabolites, siderophores, quorum sensing system, biofilm formation, and cellular transduction signaling, among others. The ultimate unit of interaction is the gene expression of each organism in response to an environmental (biotic or abiotic) stimulus, which is responsible for the production of molecules involved in these interactions. Therefore, in the present review, we focused on some molecular mechanisms involved in the microbial interaction, not only in microbial–host interaction, which has been exploited by other reviews, but also in the molecular strategy used by different microorganisms in the environment that can modulate the establishment and structuration of the microbial community.

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“…Remarkable progress in sequencing technology has advanced our understanding of particular physiological or metabolic functions in bacteria, including secondary metabolite production (11,12). For example, gene sequence homology predicts that sioxanthin biosynthesis is present in all of the Salinispora as well as in other members of the family Micromonosporaceae (11), and the clustering of carotenoid biosynthetic genes in heterotrophic bacteria reveals that gene rearrangement is common in the production of these compounds (11).…”

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confidence: 99%

Family-wide Structural Characterization and Genomic Comparisons Decode the Diversity-oriented Biosynthesis of Thalassospiramides by Marine Proteobacteria

Zhang

Liang

Lai

et al. 2016

Journal of Biological Chemistry

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Edited by Gerald W. HartThe thalassospiramide lipopeptides have great potential for therapeutic applications; however, their structural and functional diversity and biosynthesis are poorly understood. Here, by cultivating 130 Rhodospirillaceae strains sampled from oceans worldwide, we discovered 21 new thalassospiramide analogues and demonstrated their neuroprotective effects. To investigate the diversity of biosynthetic gene cluster (BGC) architectures, we sequenced the draft genomes of 28 Rhodospirillaceae strains. Our family-wide genomic analysis revealed three types of dysfunctional BGCs and four functional BGCs whose architectures correspond to four production patterns. This correlation allowed us to reassess the "diversity-oriented biosynthesis" proposed for the microbial production of thalassospiramides, which involves iteration of several key modules. Preliminary evolutionary investigation suggested that the functional BGCs could have arisen through module/domain loss, whereas the dysfunctional BGCs arose through horizontal gene transfer. Further comparative genomics indicated that thalassospiramide production is likely to be attendant on particular genes/pathways for amino acid metabolism, signaling transduction, and compound efflux. Our findings provide a systematic understanding of thalassospiramide production and new insights into the underlying mechanism.

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Elucidation of the Burkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid‐producing bacteria

Cited by 62 publications

References 68 publications

A distinct pathway for tetrahymanol synthesis in bacteria

A distinct pathway for tetrahymanol synthesis in bacteria

Microbial interactions: ecology in a molecular perspective

Family-wide Structural Characterization and Genomic Comparisons Decode the Diversity-oriented Biosynthesis of Thalassospiramides by Marine Proteobacteria

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