Interplay between arsenic and selenium biomineralization in Shewanella sp. O23S

Lucian C Staicu; Paulina J Wójtowicz; Zsombor Molnár; Encarnación Ruiz-Agudo; José Luis R Gallego; Diego Baragaño; Mihály Pósfai

doi:10.1016/j.envpol.2022.119451

Interplay between arsenic and selenium biomineralization in Shewanella sp. O23S

Environ Pollut. 2022 Aug 1:306:119451. doi: 10.1016/j.envpol.2022.119451. Epub 2022 May 12.

Authors

Lucian C Staicu¹, Paulina J Wójtowicz², Zsombor Molnár³, Encarnación Ruiz-Agudo⁴, José Luis R Gallego⁵, Diego Baragaño⁵, Mihály Pósfai³

Affiliations

¹ Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096, Warsaw, Poland. Electronic address: staicu@biol.uw.edu.pl.
² Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096, Warsaw, Poland.
³ Research Institute of Biomolecular and Chemical Engineering, University of Pannonia, Egyetem u. 10, H-8200, Veszprém, Hungary; ELKH-PE Environmental Mineralogy Research Group, University of Pannonia, Egyetem u. 10, H-8200, Veszprém, Hungary.
⁴ Department of Mineralogy and Petrology, University of Granada, Granada, Spain.
⁵ Environmental Biogeochemistry & Raw Materials Group and INDUROT, Campus de Mieres, University of Oviedo, C/Gonzalo Gutiérrez Quirós. S/N, 33600, Mieres, Spain.

PMID: 35569621
DOI: 10.1016/j.envpol.2022.119451

Abstract

Bacteria play crucial roles in the biogeochemical cycle of arsenic (As) and selenium (Se) as these elements are metabolized via detoxification, energy generation (anaerobic respiration) and biosynthesis (e.g. selenocysteine) strategies. To date, arsenic and selenium biomineralization in bacteria were studied separately. In this study, the anaerobic metabolism of As and Se in Shewanella sp. O23S was investigated separately and mixed, with an emphasis put on the biomineralization products of this process. Multiple analytical techniques including ICP-MS, TEM-EDS, XRD, Micro-Raman, spectrophotometry and surface charge (zeta potential) were employed. Shewanella sp. O23S is capable of reducing selenate (SeO₄^2-) and selenite (SeO₃^2-) to red Se(-S)⁰, and arsenate (AsO₄^3-) to arsenite (AsO₃^3-). The release of H₂S from cysteine led to the precipitation of AsS minerals: nanorod AsS and granular As₂S₃. When As and Se oxyanions were mixed, both As-S and Se(-S)⁰ biominerals were synthesized. All biominerals were extracellular, amorphous and presented a negative surface charge (-24 to -38 mV). Kinetic analysis indicated the following reduction yields: SeO₃^2- (90%), AsO₄^3- (60%), and SeO₄^2- (<10%). The mix of SeO₃^2- with AsO₄^3- led to a decrease in As removal to 30%, while Se reduction yield was unaffected (88%). Interestingly, SeO₄^2- incubated with AsO₄^3- boosted the Se removal (71%). The exclusive extracellular formation of As and Se biominerals might indicate an extracellular respiratory process characteristic of various Shewanella species and strains. This is the first study documenting a complex interplay between As and Se oxyanions: selenite decreased arsenate reduction, whereas arsenate stimulated selenate reduction. Further investigation needs to clarify whether Shewanella sp. O23S employs multi-substrate respiratory enzymes or separate, high affinity enzymes for As and Se oxyanion respiration.

Keywords: Arsenic; Biominerals; Environmental pollution; Selenium; Shewanella.

MeSH terms

Arsenates / metabolism
Arsenic* / metabolism
Biomineralization
Kinetics
Selenic Acid
Selenious Acid
Selenium Compounds*
Selenium* / metabolism
Shewanella* / metabolism

Substances

Arsenates
Selenium Compounds
Selenious Acid
Selenium
Selenic Acid
Arsenic