Abstract
Digestion-resistant bacteria (DRB) refer to the ecological bacterial group that can be ingested, but not digested by protistan grazers, thus forming a specific type of bacteria-protist association. To test the hypothesis that the environment affects the assembly of DRB in protists, a mixotrophic ciliate, Paramecium bursaria, and a heterotrophic ciliate, Euplotes vannus, were reared at different temperatures, light conditions, and concentration gradients of antibiotic oxytetracycline and heavy metals. Community profiling indicated that the composition of DRB in both species varied significantly across the manipulated conditions, except for in P. bursaria under light/dark treatments. Clone library analysis of bacterial 16S rRNA genes showed that DRB were diverse. Pseudomonas became more abundant during the warmer treatment of P. bursaria, whereas the dominance of Pseudoalteromonas weakened and Vibrio became more abundant in E. vannus at a higher temperature. During the treatment of diel light:dark cycles, Aestuariibacter and Alteromonas were selected for in E. vannus but not Pseudoalteromonas, which was highly represented in the all-light and alldark treatments. In contrast, P. bursaria consistently hosted Nevskia, Curvibacter, and Asticcacaulis under all light conditions. There were many bacterial species co-resistant to oxytetracycline and to protistan digestion, in which Sphingomonas, Alteromonas, Aestuariibacter, Puniceicoccaceae (Verrucomicrobia), Pseudomonas, and Sulfitobacter were frequently abundant. Flectobacillus and Aestuariibacter were major lead-resistant bacteria associated with the studied protists. Acinetobacter and Hydrogenophaga were abundant in the P. bursaria treated with a high dose of mercury. Aestuariibacter was found as a dominant group of DRB in E. vannus across all cadmium treatments. In summary, this study demonstrates for the first time that environmental stress selects for bacterial populations associated with protists and that there are diverse bacterial species that not only are resistant to pollution stresses but can also survive protistan predation. This work highlights that bacteria-protists associations need to be taken into account in understanding ecological and environmental issues, such as resilience of bacterial community and function, microbial co-occurrence, and quantity and distribution of antibiotic resistant bacteria and genes.
Highlights
Bacteria and protists are major players in the microbial food web of aquatic environments, in which heterotrophic bacteria incorporate dissolved organic matter and nutrients for growth and transfer carbon and energy to higher trophic levels as a consequence of predation by small protists (Azam et al, 1983)
We aimed to test the following hypotheses: (1) warming, light condition, antibiotic, and heavy metal treatments would individually lead to significant changes in digestion-resistant bacteria (DRB) assemblages of both ciliate species; (2) the changes in DRB assemblages in both ciliates were greater than the free-living bacterioplankton in the media; and (3) there were diverse bacteria co-resistant to antibiotics/metals and protistan digestion
The T-restriction fragment length polymorphism (RFLP) profiling and analysis of similarity (ANOSIM) results of global tests showed that all environmental factors investigated in this study, i.e., temperature (R ≥ 0.71, P ≤ 0.014), light (R ≥ 0.38, P ≤ 0.039), OTC (R ≥ 0.47, P = 0.001), Pb (R ≥ 0.75, P ≤ 0.002), Hg (R = 1.00, P = 0.001), and Cd (R = 0.76, P = 0.001), significantly affected the community structure of bacterioplankton in the culture media for the tested ciliate species (Table 1)
Summary
Bacteria and protists are major players in the microbial food web of aquatic environments, in which heterotrophic bacteria incorporate dissolved organic matter and nutrients for growth and transfer carbon and energy to higher trophic levels as a consequence of predation by small protists (Azam et al, 1983). Recent studies have provided evidence for another strategy of anti-predation—some bacterial populations in aquatic environments can be ingested, but not digested by protistan grazers, potentially forming microbial associations with the protistan hosts (e.g., First et al, 2012; Šimek et al, 2013; Gong et al, 2014). From an ecological point of view, the existence of DRB could prevent organic matter and energy from being transferred to protistan grazers and higher trophic levels via the microbial loop, adding another layer of complexity in the structure and functions of microbial webs
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