Abstract

Acidobacteria represents one of the most dominant bacterial groups across diverse ecosystems. However, insight into their ecology and physiology has been hampered by difficulties in cultivating members of this phylum. Previous cultivation efforts have suggested an important role of trace elements for the proliferation of Acidobacteria, however, the impact of these metals on their growth and metabolism is not known. In order to gain insight into this relationship, we evaluated the effect of trace element solution SL10 on the growth of two strains (5B5 and WH15) of Acidobacteria belonging to the genus Granulicella and studied the proteomic responses to manganese (Mn). Granulicella species had highest growth with the addition of Mn, as well as higher tolerance to this metal compared to seven other metal salts. Variations in tolerance to metal salt concentrations suggests that Granulicella sp. strains possess different mechanisms to deal with metal ion homeostasis and stress. Furthermore, Granulicella sp. 5B5 might be more adapted to survive in an environment with higher concentration of several metal ions when compared to Granulicella sp. WH15. The proteomic profiles of both strains indicated that Mn was more important in enhancing enzymatic activity than to protein expression regulation. In the genomic analyses, we did not find the most common transcriptional regulation of Mn homeostasis, but we found candidate transporters that could be potentially involved in Mn homeostasis for Granulicella species. The presence of such transporters might be involved in tolerance to higher Mn concentrations, improving the adaptability of bacteria to metal enriched environments, such as the decaying wood-rich Mn environment from which these two Granulicella strains were isolated.

Highlights

  • Despite being widespread and dominant in soil ecosystems (Kuramae et al, 2012; Navarrete et al, 2013b; Pereira de Castro et al, 2016), the phylum Acidobacteria has a low number of cultivated representatives, due to difficulties in isolation and propagation under laboratory conditions (Dedysh and Yilmaz, 2018)

  • We evaluated the effect of trace element addition on the growth of two strains of Granulicella, belonging to phylum Acidobacteria class “Acidobacteriia.” We observed that the growth in liquid medium of both strains was improved by the addition of Mn, to which the strains tolerated relatively higher concentrations in comparison to other metal salts

  • Variations in tolerance to metal salt concentrations suggest that the Granulicella spp. 5B5 and WH15 possess different mechanisms to deal with metal ion homeostasis and stress, reflecting the low similarity observed in the genome alignment between both strains

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Summary

Introduction

Despite being widespread and dominant in soil ecosystems (Kuramae et al, 2012; Navarrete et al, 2013b; Pereira de Castro et al, 2016), the phylum Acidobacteria has a low number of cultivated representatives, due to difficulties in isolation and propagation under laboratory conditions (Dedysh and Yilmaz, 2018). Trace elements can be used to improve microbial growth and gain of biomass under laboratory conditions, even though the specific requirements among strains and species are variable (Banerjee et al, 2009; Merchant and Helmann, 2012). Metal ions such as Fe, Mn, Zn, and Cu are fundamental for microbial metabolism, being required at low concentrations (Abbas and Edwards, 1990). They play an important role in biological processes, acting as co-factors of enzymes (Wintsche et al, 2016), activating metalloregulators and trace element dependent proteins (Hantke, 2001; Zhang et al, 2009), forming functional complexes with secondary metabolites (Morgenstern et al, 2015; Locatelli et al, 2016) and promoting the detoxification of reactive oxygen species (ROS) (Kehres and Maguire, 2003; Locatelli et al, 2016)

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