Evaluating Metabolic Pathways and Biofilm Formation in Stenotrophomonas maltophilia

Abstract

Stenotrophomonas maltophilia has recently arisen as a prominent nosocomial pathogen because of its high antimicrobial resistance and ability to cause chronic respiratory infections. Often the infections are worsened by biofilm formation which enhances antibiotic tolerance. We have previously found that mutation of the gpmA gene, encoding the glycolytic enzyme phosphoglycerate mutase, impacts the formation of this biofilm on biotic and abiotic surfaces at early timepoints. This finding, indicating an association between carbon source and biofilm formation, led us to hypothesize that metabolism would influence S. maltophilia biofilm formation and planktonic growth. In the present study, we tested the impact of various growth substrates on biofilm levels and growth kinetics to determine metabolic requirements for these processes. We found that S. maltophilia wildtype preferred amino acids versus glucose for planktonic and biofilm growth and that gpmA deletion inhibited growth in amino acids. Furthermore, supplementation of the Δ gpmA strain by glucose or ribose phenotypically complemented growth defects. These results suggest that S. maltophilia shuttles amino acid carbon through gluconeogenesis to an undefined metabolic pathway supporting planktonic and biofilm growth. Further evaluation of these metabolic pathways might reveal novel metabolic activities of this pathogen. Importance Stenotrophomonas maltophilia is a prominent opportunistic pathogen that often forms biofilms during infection. However, the molecular mechanisms of virulence and biofilm formation are poorly understood. The glycolytic enzyme phosphoglycerate mutase appears to play a role in biofilm formation, and we used a mutant in its gene ( gpmA ) to probe the metabolic circuitry potentially involved in biofilm development. The results of our study indicate that S. maltophilia displays unique metabolic activities, which could be exploited for inhibiting growth and biofilm formation of this pathogen.

Comparative Proteomic Analysis of Protein Patterns of Stenotrophomonas maltophilia in Biofilm and Planktonic Lifestyles

“…The induced expression of 2,3-bisphosphoglycerate-dependent phosphoglycerate mutase and phosphoglycerate mutase (B6314 and B7203 proteins) in biofilm samples confirmed earlier findings indicating that this glycolytic enzyme (GpmA) modulates biofilm formation in S. maltophilia on airway epithelial cells and abiotic surfaces [ 39 ]. It has been hypothesized that amino acid carbons are shuttled into the central metabolism through GpmA and toward pentose phosphate metabolism, producing an unknown compound able to stimulate growth and biofilm [ 40 ]. A greater understanding of these unique metabolic pathways is needed to define novel methods for inhibiting S. maltophilia growth and biofilm.…”

Genotypic variations and interspecific interactions modify gene expression and biofilm formation of Xanthomonas retroflexus

“…The peptide matched with a ligand‐binding sensor domain‐containing diguanylate cyclase from Stenotrophomonas spp. (cover = 100%, identity = 99.6%, E ‐value = 8.18 × 10 −70 ), whose species members are known to produce biofilm (Cierra et al, 2022). The scanning revealed the presence of multiple domains (Supporting Data 1), including: (i) a periplasmic ligand‐binding sensor domain involved in signal transduction mechanisms, (ii) a ‘Y_Y_Y’ domain of unknown function but typically found in at the end of the beta propellers in a family of two component regulators and (iii) a ‘GGDEF’ domain involved in synthesis of the c‐di‐GMP secondary messenger (c‐di‐GMP cyclase), sharing similarities with the ‘PleD superfamily’ domain characterised in the Alphaproteobacterium Caulobacter crescentus (Aldridge et al, 2003).…”

Effects of sulphur amino acids on the size and structure of microbial communities of aerobic granular sludge bioreactors

“…Regarding the presence of high concentrations of cysteine and methionine and their removal rates, they were strong and positively related to Acidovorax , Flavobacterium , Methylophilus , Stenotrophomonas , and Thauera and presented significant negative correlations with the RAs of Lacunisphaera , Parabacteroides , Pedobacter , Proteiniphilum , and Minority genera. In this sense, the growing capacity of Flavobacterium , Stenotrophomonas , and Thauera using Aa as sole substrates has been previously defined as well as their extracellular proteolytic activities (Jankiewicz et al, 2016 ; Adhikari et al, 2017 ; Gulmus and Gormez, 2020 ; Isom et al, 2021 ). On the other hand, Acidovorax and Methylophilus have not been described as proteolytic or Aa-degrading bacterium (Burdman et al, 2005 ; Jin et al, 2019 ).…”