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02 May 2024
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Maternal body condition affects the response of larval spined toads' faecal microbiome to a widespread contaminant

Effects of AMPA on Bufo spinosus microbiota

Recommended by based on reviews by Fabrice Martin-Laurent, Lauris Evariste and 1 anonymous reviewer

The overall pollution of air, water, and soil is currently recognized as one of the five main drivers of biodiversity loss (IPBES 2019). Among chemicals, pesticides play a significant role in this global crisis, as recently re-assessed at the scale of France (Pesce et al. 2023). In this context, although parent molecules are subject to national and international regulations, based on a priori ecological risk assessment (e.g., REACH) as well as monitoring in some environments (see e.g., pesticides classified in the priority list of substances by the Water Frame Directive), pesticide metabolites are rarely considered. In the case of the widely used herbicide glyphosate, a particular concern is rising about its primary metabolite, aminomethylphosphonic acid (AMPA), due to its persistence and overlooked toxicity. 

Amphibians are the most threatened class of vertebrates on earth, with two in every five species considered threatened with extinction (IUCN Red List). While this overall decline has multiple causes, the contribution of pesticides is suspected to be significant in some regions.

In this context, Tartu et al. (2024) studied the effects of AMPA on the gut microbiota of the spined toad, Bufo spinosus. This work complements a previous study which showed embryo mortality, oxidative stress, deformities at hatching, and delayed development (Tartu et al. 2022). Using a common garden experiment based on populations from contrasted habitats (agricultural vs woodland, same as in the previous study), the authors captured breeding pairs and collected the eggs laid in the laboratory. These were exposed to 0.4 µg/L AMPA during embryonic and larval development. Individual microbiota was analysed non-invasively, i.e., using the faeces collected in treatment vessels. Bacterial biodiversity was genetically assessed (16S rRNA). The community biomass and taxonomic structure were analysed as a function of chemical treatment, mother and father body condition (fat vs thin), as well as population of origin. 

As a primary effect, AMPA reduced the microbial biomass. Furthermore, a significant interaction was detected between AMPA and mother condition on the community structure and composition. This alteration, observed in « fat » females only, was reflected through a significant decrease in Bacteroidota and a significant increase in Actinobacteriota (the latter being consistent with the ability of some species in this phylum to use AMPA as a source of phosphorus). The higher sensitivity of tadpoles from females in better condition seems counterintuitive, since better body condition is expected to be associated with higher fitness (and possibly higher ability to face chemical stress), the authors discuss this in the light of the literature (which shows that microbiome-fitness relationships are not often evidenced in natural populations), and hypothesize that these females in better conditions host a microbiota that may be more efficient, yet also more sensitive to AMPA. Not ruling out other possible factors ignored in their study, in particular genotypic effects, the authors further discuss the importance of maternally transmitted effects via the microbiota. 

Altogether, the results published by Tartu et al. (2024) provide important new findings on AMPA toxicity to amphibian microbiota, and also confirm the occurrence of vertical transmission of the microbiota from mother to progeny in this vertebrate class.

References 

IPBES (2019). Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. E. S. Brondizio, J. Settele, S. Díaz, and H. T. Ngo (editors). IPBES secretariat, Bonn, Germany. 1148 pages. https://doi.org/10.5281/zenodo.3831673

Pesce, S., Mamy, L., Sanchez, W., et al. (2023). Main conclusions and perspectives from the collective scientific assessment of the effects of plant protection products on biodiversity and ecosystem services along the land–sea continuum in France and French overseas territories. Environ Sci Pollut Res . https://doi.org/10.1007/s11356-023-26952-z

Tartu, S., Renoirt, M., Cheron, M., Gisselmann, L.-L., Catoire, S., Brischoux, F. (2022). Did decades of glyphosate use have selected for resistant amphibians in agricultural habitats? Environ. Pollut. 310, 119823. https://doi.org/10.1016/j.envpol.2022.119823

Tartu, S., Pollet, N., Clavereau, I., Gauthier Bouchard, G., Brischoux, F. (2024). Maternal body condition affects the response of larval spined toads’ faecal microbiome to a widespread contaminant. bioRxiv,  ver. 2 peer-reviewed and recommended by Peer Community in Ecotoxicology and Environmental Chemistry. https://doi.org/10.1101/2023.12.18.572122

 

Maternal body condition affects the response of larval spined toads' faecal microbiome to a widespread contaminantSabrina Tartu, Nicolas Pollet, Isabelle Clavereau, Gauthier Bouchard, Francois Brischoux<p>Glyphosate’s primary metabolite, aminomethylphosphonic acid (AMPA), is the most detected pollutant in surface waters. Recent studies have raised concerns about its toxicity, yet underlying mechanisms remain poorly understood. A disruption of th...Aquatic ecotoxicology, Environmental pollutionMarie-Agnès Coutellec Lauris Evariste, Fabrice Martin-Laurent2023-12-19 10:32:45 View
29 Jul 2024
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Molecular response to multiple trace element contamination of the European sardine

Molecular-level responses highlight physiological stress in muscle and liver tissue of apparently healthy European sardine specimen

Recommended by ORCID_LOGO and ORCID_LOGO based on reviews by Sophie Prud'homme, Roberta Bettinetti and 1 anonymous reviewer

Fish is an essential component of healthy human diets and the preservation of fish stocks and other marine resources is included as a target of Sustainable Development Goal 14 ‘Conserve and sustainably use the Oceans, Sea and Marine Resources for Sustainable Development’ (UNEP). However, several fish stocks remain in sub-optimal (or worse) conditions due to overfishing and a range of stressors including chemical pollution. Chemical pollution can result in high level of chemicals in fish making it unsuitable for human consumption. Furthermore, the occurrence of chemical-related physiological stress in otherwise apparently healthy fish requires additional research efforts. In natural environments, further complexity arises from fish being simultaneously exposed to multiple contaminants/stressors as opposed to laboratory investigation usually dealing with one or very few contaminants/stressors at a time (Schäfer et al., 2023).

Beauvieux et al. (2024) examined the possible role of accumulation of multiple elements on the physiological status of first-year-of-life specimen of European sardine collected in the Gulf of Lions (northeastern Mediterranean Sea) as a contributing factor to the declining sardine population observed in the region since 2008. The ultimate objective of the paper was to identify potential biomarkers of stress in fish otherwise not exhibiting any anomalies in body condition, in agreement with the principles of chemical stress ecology put forward by van der Brink (2008). 

Out of a total of 105 specimen, individuals were selected according to the lowest (n = 14) or highest (n = 15) levels of contamination and subject to proteomic analysis of liver and red muscle tissues.  A first Principal component analysis on all specimen highlighted the possible influence of the Rhone river as a source of geogenic and anthropogenic elements to the Gulf of Lions. 

A second PCA performed only on specimen selected from proteomics analysis allowed to identify three elemental mixtures possibly responsible for the observed physiological effects. Proteomic analysis in liver and muscle tissue identified both similarities and differences in the pathways involved in response to stress. More in detail, the expression patterns of Myosin and Myomesin were downregulated in red muscle for highly exposed specimen, which suggests possible effects of elemental accumulation on the locomotion abilities of Mediterranean sardines. Pathways involved in lipid metabolism and immune processes were up-regulated in liver, pointing to increased energetic costs for maintaining the overall fish homeostasis in presence of metal contamination. It is interesting to note that these effects were observed at concentrations below the legal thresholds for human consumption (except for As), albeit such thresholds are available only for a limited number of elements (Cd, Pb, Cd, As and inorganic Sn) (EU, 2023).

Although stressors other than trace elements could contribute to the observed molecular responses, as acknowledged by the authors themselves, Beauvieux et al. (2024) show that biological responses at lower levels of biological organization can provide both early-warning indications of potential adverse effects in the long term and better understanding of drivers of population decline. By advancing our knowledge of the physiological responses to trace elements and identifying potential biomarkers, this study lays the groundwork for more effective monitoring and conservation strategies. Further studies addressing the combined effects of multiple environmental stressors remain essential to develop holistic approaches to marine ecosystem management and species conservation. 

 

References

Beauvieux A., Fromentin J.-M., Saraux C., Romero D., Couffin N., Brown A., Metral L., Bertile F., Schull Q. (2024). Molecular response to multiple trace element contamination of the European sardine. bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecotoxicology and Environmental Chemistry. https://doi.org/10.1101/2024.02.16.580673  

EU (2023). Commission Regulation (EU) 2023/915. https://eur-lex.europa.eu/eli/reg/2023/915/oj/eng

Schäfer R. B., Jackson M., Juvigny-Khenafou N., Osakpolor S. E., Posthuma L., Schneeweiss A., Spaak J., & Vinebrooke R. (2023). Chemical Mixtures and Multiple Stressors: Same but Different? Environmental Toxicology and Chemistry, 42(9), 1915-1936, https://doi.org/https://doi.org/10.1002/etc.5629

UNEP: https://sdgs.un.org/goals

Van den Brink P. J. (2008). Ecological Risk Assessment: From Book-Keeping to Chemical Stress Ecology. Environmental Science & Technology, 42(24), 8999-9004. https://doi.org/10.1021/es801991c 

Molecular response to multiple trace element contamination of the European sardineAnaïs Beauvieux, Jean-Marc Fromentin, Claire Saraux, Diego Romero, Nathan Couffin, Adrien Brown, Luisa Metral, Fabrice Bertile, Quentin Schull<p>In marine ecosystems, the presence of trace elements resulting from anthropogenic activities has raised concerns regarding their potential effects on marine organisms. This study delves into the intricate relationship between trace element cont...Biomarkers, Environmental pollution, Marine ecotoxicologyDavide Anselmo Luigi Vignati2024-02-22 16:24:52 View