Impact of Tellurite on the Metabolism of Paenibacillus pabuli AL109b With Flagellin Production Explaining High Reduction Capacity

Abstract

Tellurium (Te) is a metalloid with scarce and scattered abundance but with an increased interest in human activity for its uses in emerging technologies. As is seen for other metals and metalloids, the result of mining activity and improper disposal of high-tech devices will lead to niches with increased abundance of Te. This metalloid will be more available to bacteria and represent an increasing selective pressure. This environmental problem may constitute an opportunity to search for microorganisms with genetic and molecular mechanisms of microbial resistance to Te toxic anions. Organisms from Te-contaminated niches could provide tools for Te remediation and fabrication of Te-containing structures with added value. The objective of this study was to determine the ability of a high metal-resistant Paenibacillus pabuli strain ALJ109b, isolated from high metal content mining residues, to reduce tellurite ion, and to evaluate the formation of metallic tellurium by cellular reduction, isolate the protein responsible, and determine the metabolic response to tellurite during growth. P. pabuli ALJ109b demonstrated to be resistant to Te (IV) at concentrations higher than reported for its genus. It can efficiently remove soluble Te (IV) from solution, over 20% in 8 h of growth, and reduce it to elemental Te, forming monodisperse nanostructures, verified by scattering electron microscopy. Cultivation of P. pabuli ALJ109b in the presence of Te (IV) affected the general protein expression pattern, and hence the metabolism, as demonstrated by high-throughput proteomic analysis. The Te (IV)-induced metabolic shift is characterized by an activation of ROS response. Flagellin from P. pabuli ALJ109b demonstrates high Te (0) forming activity in neutral to basic conditions in a range of temperatures from 20°C to 37°C. In conclusion, the first metabolic characterization of a strain of P. pabuli response to Te (IV) reveals a highly resistant strain with a unique Te (IV) proteomic response. This strain, and its flagellin, display, all the features of potential tools for Te nanoparticle production.

Potential of tellurite resistance in heterotrophic bacteria from mining environments

“…The formation of string-like deposits of Te in the case of B. safensis 10W7 and B. altitudinis 3W19 is indicative of template base formation of nanoparticles on cell structures, i.e. the flagellum, like what is suggested for P. pabuli ALJ109b ( Farias et al., 2021 ). Shard/rod-like structures, observed in B. altitudinis 3W19 and C. marina 5W10, were previously observed in Pseudomonas putida strain BS228 ( Suzina et al., 1995 ), in Pseudomonas pseudoalcaligenes strain Te ( Forootanfar et al., 2015 ) or in Bacillus selenitireducens and Sulfurospirillum barnesii ( Baesman et al., 2007 ), indicating that these geometries are common in Te-containing nanostructures.…”

“…In Paenibacillus , although there are no publicly available reports concerning Te r mechanisms, considering the phylogenetic proximity of the two taxa, likely resistant strains of Paenibacillus were also able to reduce Te (IV). Our previous study describes in detail the ability of Paenibacillus pabuli ALJ109b, from Aljustrel, to reduce Te (VI) using flagellin ( Farias et al., 2021 ). Most of the recognized Te r genetic determinants were not found in this strain, and those that were found did not display the usual organization of Te (IV) resistance gene clusters or operons.…”

Microbial mechanisms to transform the super-trace element tellurium: a systematic review and discussion of nanoparticulate phases

“…Additionally, a 117 kDa membrane protein in E. ursincola KR99 (Maltman et al 2017a ), TrxR in Bacillus sp. Y3 (Yasir et al 2020 ), Mycothione reductase in Rhodococcus erythropolis PR4 (Butz et al 2020 ) and Flagellin (FlaA) in Paenibacillus pabuli ALJ109b (Farias et al 2021 ) were also proven to be acting as microbial tellurite reductases.…”