MAHAMOUD-AHMED Ayanleh
2016-2021
Impact of Sediment Contamination on the Diversity, Functional Potential, and Tolerance Capacity of Benthic Microbial Communities
Supervisors: Emilie Lyautey (USMB, UMR CARRTEL) and Stéphane Pesce (Irstea, UR RiverLy)
Doctoral School: SISEO, University of Savoie Mont Blanc, Grenoble Alpes University Community

The aim of this thesis is to strengthen the ecological and ecotoxicological studies of sediment compartments by understanding the impacts of model contaminants on benthic microbial communities. The results demonstrate that environmental concentrations of certain metals, such as copper, can significantly impact microbial biodiversity and several ecological functions performed by microorganisms. Moreover, the study highlights microbial adaptation capacity, which results in increased tolerance at the community level, opening up possibilities for applying the Pollution Induced Community Tolerance (PICT) approach as a bio-indicator tool for ecotoxicological impacts in sediment compartments.

While many contaminants accumulate in the sediment compartments of aquatic ecosystems, knowledge on how natural sediment communities respond to this contamination remains scarce. This is particularly true for benthic microbial communities, which play a crucial ecological role in this compartment.
This thesis project aims to assess the impacts of polychlorinated biphenyls (PCBs) and trace metal elements (ETMs) on natural benthic microbial communities using experimental approaches in microcosms, including column setups (for lake surface sediments) and artificial channels (for river surface sediments), respectively (see illustrations). Using arochlor 1254 as the model contaminant for PCBs (column experiment), and copper (Cu) and arsenic (As) for ETMs (channel experiment), the project aims to:
i) characterize the functional and structural responses of benthic microbial communities exposed to realistic environmental concentrations, and
ii) understand their adaptation capacity to chronic exposure.

The results show that PCBs and As have no effect on any of the measured community effect descriptors for sediment microbial communities. However, in the presence of Cu (either alone or mixed with As), significant and immediate effects are observed on most of the measured functions, including various enzymatic activities involved in the degradation of organic carbon, nitrogen, and phosphate compounds, as well as metabolic activities such as respiration and denitrification. Analysis of microbial community diversity (bacteria and archaea) also indicates significant and rapid effects from Cu, leading to a restructuring of the community. This restructuring is reflected in the reduction of species richness and a decrease in the evenness between taxa. Statistical analysis helped identify the main taxa responsible for the observed changes, grouping species that are negatively affected (potentially sensitive) and those that are favored (directly and/or indirectly) by the presence of Cu. To assess the consequences of these community shifts on their tolerance to Cu, we used a Pollution Induced Community Tolerance (PICT) approach with acute toxicity tests on enzymatic activities. The increase in EC50 values for communities exposed to Cu confirms the development of tolerance at the community level due to the selection of tolerant species. Furthermore, the absence of an increase in the abundance of the cusA gene (which is involved in Cu resistance) in the exposed communities suggests that tolerance acquisition is not linked to an increase in the genetic potential associated with this process. This will be further verified by quantifying a second Cu resistance gene (copA) and genes coding for ETM efflux pumps (HME-RND family) in the exposed communities.

Mahamoud Ahmed - Fig1
Experimental setups used with lake sediments (A) and river sediments (B).

In summary, the results of this study show that environmental concentrations of Cu (and likely other ETMs) can impact the functional potential and diversity of benthic microbial communities, inducing the acquisition and development of tolerance capabilities to this metal through the selection of tolerant taxa at the expense of the more sensitive ones.

Consequently, due to the significant role of benthic microbial communities in biogeochemical cycles, these functional and structural modifications could have important repercussions on the overall functioning of aquatic ecosystems. Additionally, the observed acquisition of tolerance in exposed communities opens up prospects for using the PICT approach in the sediment compartment as a tool for bio-surveillance to assess ecotoxicological impacts in contaminated natural environments.

 Publication

  • MAHAMOUD AHMED A., LYAUTEY E., BONNINEAU C., DABRIN A., PESCE S. (2018). Environmental concentrations of copper, alone or in mixture with arsenic, can impact river sediment microbial community structure and functions. Front. Microbiol. 9:1852. https://doi.org/10.3389/fmicb.2018.01852

Communications at International Congresses

  • MAHAMOUD AHMED A., LYAUTEY E., DABRIN A., BONNINEAU C., GAHOU J., MOTTE B., ROSY C., VOLAT B., PESCE S. (2017). Structural and functional response of river sediment microbial communities to environmental concentrations of copper and arsenic, alone or in mixture. 1st International Conference on Microbial Ecology - EcotoxicoMic, Lyon, France, 21-24 novembre 2017 (Poster).
  • MAHAMOUD AHMED A., PESCE S., NAFFRECHOUX E., COTTIN N., BONNINEAU C., VOLAT B., LYAUTEY E. (2017). Natural lake sediment microbial community response to exposure to environmental PCB concentrations in microcosms. 1st International Conference on Microbial Ecotoxicology, Lyon, 21-24 novembre 2017 (Poster).
  • MAHAMOUD AHMED A. PESCE S., DABRIN A., GAHOU J., MOTTE B., ROSY C., VOLAT B., LYAUTEY E. (2017). Combined effects of environmental concentrations of copper and arsenic on natural river sediment microbial communities. 14th International AquaConSoil Conference, Lyon, France, 26 - 30 Juin 2017 (Communication orale).
  • MAHAMOUD AHMED A., LYAUTEY E., DABRIN A., MOTTE B., ROSY C., VOLAT B., PESCE S. (2017). Structural and functional response of natural river sediment microbial communities to environmental concentrations of copper and arsenic, alone or in mixture. SETAC Europe 27th Annual Meeting, Bruxelles, Belgique, 7 - 11 Mai 2017 (Poster corner).