Graphene-Based Nanomaterials Modulate Internal Biofilm Interactions and Microbial Diversity

Abstract

Graphene-based nanomaterials (GBMs), such as graphene oxide (GO) and reduced graphene oxide (rGO), possess unique properties triggering high expectations for the development of new technological applications and are forecasted to be produced at industrial-scale. This raises the question of potential adverse outcomes on living organisms and especially toward microorganisms constituting the basis of the trophic chain in ecosystems. However, investigations on GBMs toxicity were performed on various microorganisms using single species that are helpful to determine toxicity mechanisms but fail to predict the consequences of the observed effects at a larger organization scale. Thus, this study focuses on the ecotoxicological assessment of GO and rGO toward a biofilm composed of the diatom Nitzschia palea associated to a bacterial consortium. After 48 and 144 h of exposure to these GBMs at 0, 0.1, 1, and 10 mg.L−1, their effects on the diatom physiology, the structure, and the metabolism of bacterial communities were measured through the use of flow cytometry, 16S amplicon sequencing, and Biolog ecoplates, respectively. The exposure to both of these GBMs stimulated the diatom growth. Besides, GO exerted strong bacterial growth inhibition as from 1 mg.L−1, influenced the taxonomic composition of diatom-associated bacterial consortium, and increased transiently the bacterial activity related to carbon cycling, with weak toxicity toward the diatom. On the contrary, rGO was shown to exert a weaker toxicity toward the bacterial consortium, whereas it influenced more strongly the diatom physiology. When compared to the results from the literature using single species tests, our study suggests that diatoms benefited from diatom-bacteria interactions and that the biofilm was able to maintain or recover its carbon-related metabolic activities when exposed to GBMs.

Graphene-based nanomaterials and microbial communities: a review of their interactions, from ecotoxicology to bioprocess engineering perspectives

“…A beneficial effect of GO at 10 mg L −1 on the growth rates of diatoms was measured in a diatom–bacteria biofilm. 70 In this same study, bacteria growth rate was decreased, showing contrasted effects of GO on different organisms in one same community. Taken as a whole, these results suggest an adaptivity or even a growth stimulation of some microorganisms at lower doses of graphene.…”

“…55 In a biofilm composed of diatoms and bacteria, the bacterial growth rate was found to be highly diminished compared to the control (up to 75%) by the presence of 1 and 10 mg L −1 of GO after 48 and 144 h of exposure, whereas rGO impacted only slightly the growth rate at 10 mg L −1 . 70 This study highlighted different effects of different GBMs on the same community. Like reported on monocultures of bacteria, 16 the overall oxidative stress was enhanced in microbial communities exposed to GBMs 33,50,66 which could explain the observed negative effects on the growth rates in these different studies.…”

“…The different types of soils studied were the following: paddy, 54 urban, 55,56 agriculture, [57][58][59][60][61][62] forest, 63 mountain 64 and grassland 65 soils. The aquatic environment was also studied using communities from surface waters such as rivers, 66,67 lake, 66 estuary 68 and aquarium 69,70 but also sediment communities. 71,72 Those communities were exposed to GBMs in microcosm experiments of variable size, complexity and realism.…”

“…4.2.2 Degradation of organic matter. Evariste et al 70 measured potential activities related to organic matter degradation in aquatic microbial community exposed to 0.1, 1 and 10 mg L −1 of rGO and GO. The authors revealed an increase of the specific activity of the communities exposed to 10 mg L −1 of GO for 48 hours.…”

“…53 The degradation of graphene by different microbial peroxidase enzymes was also highlighted: lignin peroxidase produced by white rot fungus 93 but also horseradish peroxidase and myeloperoxidase. 24 Furthermore, in the presence of graphene, the relative abundance of bacterial strains capable of the biodegradation of complex carbon pollutants were found to be enhanced, 34,54,64,70 suggesting that this capacity of biodegradation could also be effective on GBMs. To our knowledge, this oxidative activity has not been demonstrated in complex communities.…”