Impact of land use on sediment and mayfly larval prokaryotic communities in temperate freshwater ecosystems

Host-microbe interactions are key for host health, behavior and function. Besides vertical transmission, hosts acquire part of their microbiome from the surrounding environment. Thus, environmental microbiome alterations can disrupt host microbial communities and may induce dysbiosis. We hypothesized that intensive land use resulting in increased nutrient runoff and suspended organic matter (SOM) would impact the microbiome of sediments (< 5 cm in depth) and mayfly larvae hosts (Ephemera danica) feeding on SOM within the sediment. The prokaryotic communities of sediment and mayfly larvae guts were analyzed in relation to land use gradients including forest, extensive grassland and intensive agriculture of two different stream catchments (Otterbach and Perlenbach) in the Forstmühler Forest, Upper Palatinate, Germany.

Five sediment replicates and larvae samples were collected from each site at two time points in 2023 (August and November). Three dissected larvae guts were pooled for each replicate, resulting in five biological replicates per site. Prokaryotic community composition was assessed through 16S rRNA gene amplicon sequencing. Sequencing results were processed with DADA2 v1.28.0 until the obtention of amplicon sequencing variants (ASVs), which were taxonomically classified using the Silva v138.1 database.

Nutrient gradients played a significant role in shaping beta-diversity, particularly in sediment samples. PERMANOVA tests indicated that sampling time and land use significantly influenced clustering within sample types. The analysis of compositions of microbiomes with bias correction 2 method was used to detect differentially abundant ASVs comparing forest and intensive site samples for each sample type. This approach identified potentially pathogenic, fertilization and sewage-associated taxa in the larvae gut and sediment samples from the site under intensive management, such as Aeromonas, Gaiella, Illumatobacter or Terrimonas, which can harbor type VI secretion systems, antimicrobial resistance or denitrification, while taxa with beneficial properties, such as Anaerovorax, Lachnospiraceae or Christensenellaceae, typically known as short-chain fatty acids producers and plant material degraders, were detected in the forest site larvae guts.

Our findings demonstrate downstream effects of terrestrial land use on freshwater ecosystems, with potentially negative effects on host-microbe interactions, entailing loss of function or behavioral changes.