Metal resistance systems in cultivated bacteria: are they found in complex communities?
Graphical abstract
Introduction
Bacterial adaptations to excessive concentrations of metals have been described in many cultivated species [e.g., 1•]. A total of 22 systems are known and concern the extracellular environment, the outer membrane, the periplasm, the cytoplasmic membrane and the cytoplasm (Figure 1, Table 1). However, microbial ecosystems are often complex, with many uncultivated bacteria. As a consequence, resistance systems described in cultivated strains are not necessarily used or widespread in complex communities. The knowledge of the most widespread systems is important, particularly in the field of ecotoxicology where metal resistance genes may be used as bioindicators of metal pollution [2]. To get a clearer picture, recent studies focused on metal-contaminated bacterial communities were reviewed. Only studies using shotgun metagenomics (6 studies) and metatranscriptomics (1 study) were selected because these approaches circumvent PCR biases [3]. These studies encompass 9 sites (Table S2). Two of the considered studies also used metaproteomics. Below, the possible resistance systems are listed and in each case it is indicated if their characteristic genes (when known) were found in the selected studies (Table 1, B).
Section snippets
Biogenic sulfides and other extracellular minerals
It is known for a long time that dissolved metals may be removed from solution by the production of biogenic sulfides. For instance, in a metal-contaminated salt marsh it was shown that the most active zone of sulfate-reduction controlled metal speciation [4]. At the community level, it was recently observed in lake sediments that sulfate reduction genes (dsr) were more abundant than other gene categories and were highly correlated with metal contamination [5]. Similarly, in a
The extracellular polymeric substances (EPS)
The EPS of bacteria are known to complex metals [20] and protect them from excessive metal stress [21, 22]. Once complexed, particular minerals may nucleate [23, 24] a process that gives additional protection, particularly for Fe/Mn oxyhydroxides [25, 26]. At the community level, it was shown that the most significant difference between a metal-contaminated sediment and a less contaminated site concerned the SEED gene category [27] ‘cell wall and capsule’ that included among others a glycosyl
The outer membrane (OM) in Gram-negatives
Lipopolysaccharides (LPS) in the OM have been proposed to be involved in metal resistance as they may nucleate minerals [15]. An important enzyme in LPS formation is KDO-8-P synthase (i.e., 3-deoxy-8-phosphooctulonate synthase), an enzyme that produces an anionic sugar (3-deoxy-a-D-manno-oct-2-ulosonic acid, or KDO) located in the inner core of LPS [29]. In a metal-contaminated sediment it was found that levels of the KDO-8-P synthase were high in comparison to sediments much less contaminated [
Periplasmic proteins
A series of metal-binding proteins have been described in the periplasm. For Cu, CusF was found in E. coli [43], CueP in Salmonella typhimurium [44], CopK in C. metallidurans CH34 [45•] and CopM in Synechocystis sp. PCC 6803 [46]. In a metagenomic study [10••], high levels of copK were found in activated sludge of a tannery wastewater treatment plant containing low levels of Cu.
Periplasmic redox enzymes are also found. For Cu, this category includes multicopper oxidases such as CueO or CuiD [47
The electron transport chains and phosphatases
Metals may be directly oxidized or reduced by enzymes of the electron transport chains, a process that may lead to mineral formation in the periplasm or the cytoplasm like for tellurite [59, 60]. At the community level, metaproteomics indicated that the respiration SEED category was significantly increased in a metal-contaminated sediment when compared to a less contaminated site [9••]. Lipid phosphatases may also be used to precipitate metal phosphate phases in the periplasm. The best example
Redox changes
Redox changes may detoxify metals in the cytoplasm such as As, Sb, Cr, Hg, Se and Te. For instance, ArsC reduces As(V) to As(III) [68] and the arsenite oxidase AioA may be used to oxidize As(III) [69]. ArsH is another cytoplasmic protein that confers resistance to organoarsenicals [70]. For Cr, specialized Cr(VI) reducing enzymes (reductases) have been found in some bacteria and several components of the cytoplasm also reduce Cr(VI) such as NADH, flavoproteins and other hemeproteins [71]. For
Conclusions
Of the 22 systems listed in Table 1 (column A) only 14 were detected in complex communities (Table 1, column B). This means that 8 systems may be of less importance at the community level and that their genes should not be targeted in ecotoxicological studies. However, it has to be remembered that all genes involved in resistance systems are not necessarily known. For instance, this is the case for the generation of outer membrane vesicles or the accumulation of minerals in the cytoplasm. On
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
This work was supported by FNRS grants (FRFC Nr 2.4577.12, PDR 19545408) and a Belgian IAP research network (MRM μ-manager, Belspo P7/25). Many thanks to the reviewers for their criticism and suggestions.
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