Microbially-mediated indirect effects of silver nanoparticles on aquatic invertebrates

Abstract

Complex natural systems are affected by multiple anthropogenic stressors, and therefore indirect effects within food webs are increasingly investigated. In this context, dead organic matter (OM) or detritus provides a food source sustaining detrital food webs that recycle the retained energy through microbial decomposition and invertebrate consumption. In aquatic environments, poorly water-soluble contaminants, including nanoparticles (NPs), quickly adsorb onto OM potentially modifying OM-associated microbial communities. Since invertebrates often depend on microbial conditioning to enhance OM quality, adverse effects on OM-associated microbial communities could potentially affect invertebrate performances. Therefore, this study assessed the effect of environmentally relevant concentrations of the model emerging contaminant, silver nanoparticles (AgNPs), on OM-associated microorganisms and subsequent indirect effects on growth of the invertebrate Asellus aquaticus. At low concentrations (0.8 ug/L), AgNPs inhibited activity and altered metabolic diversity of the OM-associated microbial community. This was observed to coincide with a negative effect on the growth of A. aquaticus due to antimicrobial properties, as a decreased growth was observed when offered AgNP-contaminated OM. When A. aquaticus were offered sterile OM in the absence of AgNPs, invertebrate growth was observed to be strongly retarded, illustrating the importance of microorganisms in the diet of this aquatic invertebrate. This outcome thus hints that environmentally relevant concentrations of AgNPs can indirectly affect the growth of aquatic invertebrates by affecting OM-associated microbial communities, and hence that microorganisms are an essential link in understanding bottom-up directed effects of chemical stressors in food webs.

Significance of sunlight for organic matter degradation in aquatic systems

“…phenolic content) also seems to negatively affect microbial resource niche breadth. The observed negative effects of sunlight on OM-associated microbial communities also likely reduce overall microbial respiratory activity and microbial biomass production, which itself may already retard microbiallymediated OM degradation (Tlili et al 2017) and growth of invertebrates that consume microbially-conditioned OM (Zhai et al 2018).…”

“…Secondly, it is known that sunlight can directly impair microbial communities through detrimental effects on DNA and extracellular enzymes (Santos et al 2013), or indirectly affect OM-associated microbial communities via photodegradation of OM into smaller palatable or harmful molecules depending on OM substrate (Mopper and Zhou 1990, Scully et al 1996, Obernosterer and Benner 2004, Hunting et al 2013a. This can be particularly relevant as besides their direct role in decomposing OM (Amado et al 2007), microbial communities also form an essential link towards invertebrates feeding on the OM by enhancing palatability and provisioning of nutrients (Graça et al 1993, Graça 2001, Danger and Robson 2004, Zhai et al 2018. Several invertebrates can detect resulting differences in food quality and select the most palatable food Graça 2008, Hunting et al 2013a), and adverse effects of sunlight on OM-associated biofilms have been observed to impair invertebrate growth (Franken et al 2005, Albarino et al 2008.…”

The Chemical Transformation of the Cellular Toxin INT (2-(4-Iodophenyl)-3-(4-Nitrophenyl)-5-(Phenyl) Tetrazolium Chloride) as an Indicator of Prior Respiratory Activity in Aquatic Bacteria

“…Martínez-García et al (2009) [4] showed that in eukaryotes, the formazan production is only stopped after several hours, indicating a delayed toxic effect. The ETS vivo method as it has been applied up to this day as a rate measurement [4,17,18,19] presents several potential problems: INT is toxic because it interferes with the respiration chain in prokaryotes and eukaryotes, the kinetics of poisoning for prokaryotes and eukaryotes have very different time scales, but in mixed natural populations they occur simultaneously in the same sample, and apart from the respiratory chain other cell components might also reduce INT [20,21].…”

Emerging contaminants affect the microbiome of water systems—strategies for their mitigation

“…Pharmaceuticals have been the ECs more studied 42,45,59,61 , and less importance has been given to the effects of personal care products, plasticizers, perfluorinated compounds, pesticides, and other worrying ECs commonly found in water sources. Some works reported the effects of NPs in microbial behavior [62][63][64][65][66] , however, most of these studies did not focus on biofilms but on ecotoxicological tests using planktonic microorganisms [64][65][66] . Supplementary Table 2 summarizes some works that evaluated the effects of ECs on the microbiome of water systems, reporting the exposure conditions and the main effects observed.…”