Abstract
Plasmids carrying metal resistance genes (MRGs) have been suggested to be key ecological players in the adaptation of metal-impacted microbial communities, making them promising drivers of bio-remediation processes. However, the impact of metals on plasmid-mediated spread of MRGs through selection, plasmid loss, and transfer is far from being fully understood. In the present study, we used two-member bacterial communities to test the impact of lead on the dispersal of the IncP plasmid pKJK5 from a Pseudomonas putida KT2440 plasmid donor and two distinct recipients, Variovorax paradoxus B4 or Delftia acidovorans SPH-1 after 4 and 10 days of mating. Two versions of the plasmid were used, carrying or not carrying the lead resistance pbrTRABCD operon, to assess the importance of fitness benefit and conjugative potential for the dispersal of the plasmid. The spread dynamics of metal resistance conveyed by the conjugative plasmid were dependent on the recipient and the lead concentration: For V. paradoxus, the pbr operon did not facilitate neither lead resistance nor variation in plasmid spread. The growth gain brought by the pbr operon to D. acidovorans SPH-1 and P. putida KT2440 at 1 mM Pb enhanced the spread of the plasmid. At 1.5 mM Pb after 4 days, the proteomics results revealed an oxidative stress response and an increased abundance of pKJK5-encoded conjugation and partitioning proteins, which most likely increased the transfer of the control plasmid to D. acidovorans SPH-1 and ensured plasmid maintenance. As a consequence, we observed an increased spread of pKJK5-gfp. Conversely, the pbr operon reduced the oxidative stress response and impeded the rise of conjugation- and partitioning-associated proteins, which slowed down the spread of the pbr carrying plasmid. Ultimately, when a fitness gain was recorded in the recipient strain, the spread of MRG-carrying plasmids was facilitated through positive selection at an intermediate metal concentration, while a high lead concentration induced oxidative stress with positive impacts on proteins encoding plasmid conjugation and partitioning.
Highlights
Metals constitute a serious risk for ecosystems because of their biotoxicity and bioaccumulation
The growth rate of D. acidovorans SPH-1/pKJK5gfp was significantly decreased at high lead concentrations (Pb1 and Pb-1.5)
The cost imposed by the pbr operon would be larger than the benefit it procured to the host
Summary
Metals constitute a serious risk for ecosystems because of their biotoxicity and bioaccumulation. Horizontal gene transfer, especially when mediated by plasmids, was proposed as a mechanism involved in the resilience of microbial communities in metal-impacted ecosystems (Jacquiod et al, 2018; Cyriaque et al, 2020b). Plasmids are considered key players in bacterial adaptation, as they mobilize genes contributing to genome innovation (Norman et al, 2009) Their persistence in a community is dependent on (i) their acquisition rate (conjugation and transformation), (ii) their fitness (i.e., ability to survive in a competitive environment) cost/benefit on their host, and (iii) loss rate (stability) (Bahl et al, 2009; Lopatkin et al, 2017). Metals were shown to decrease plasmid dispersal in a soil microbial community without impacting the diversity of transconjugants (Klümper et al, 2017). Our initial hypothesis was that the plasmid-encoded lead resistance system would facilitate the spread of the plasmid in a metalimpacted environment
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