Longer projected droughts will impair the recovery of tropical seedlings and their leaf microbiota

Abstract

The increasingly severe droughts in the Amazon Basin make it urgent to understand the resilience of tropical tree species and their microbiota. Plant-associated fungi and bacteria (i.e. extended phenotype) modulate drought stress for their hosts, but their role in recovery dynamics remains poorly understood. To test the impact of different drought durations on the recovery of both physiology and microbiota of tropical trees, we followed the responses of nearly 1,000 seedlings belonging to seven tropical tree species of seasonally flooded (SF) forests in a greenhouse experiment. Seedlings were subjected to different droughts, reflecting a current, a projected and an extreme drought scenario of the French Guiana climate. Plant responses were monitored after the drought and after rewetting. Plant performance was estimated through leaf gas exchange, photochemical functioning, leaf water potentials and water-related traits as well as morphological traits. Bacterial and fungal leaf communities were characterized with respectively 16S and ITS2 markers using high-throughput sequencing. Increasing the duration of the drought reduced the ability of plants to recover physiological functions, with differences among species which were only partially predicted by their drought tolerance strategies. Bacterial diversity increased in most plant host species after mild drought but not under the most severe stress. Bacterial dispersion and turnover responses were strongly host species-specific, without a general directional pattern across species. Fungal communities showed greater compositional stability, but exhibited consistently higher turnover compared to bacterial communities during both drought and recovery, with no convergence toward control composition. Finally, none of the recovery networks mirrored the architecture of the control network, regardless of prior drought duration, demonstrating that the integrated extended phenotype does not recover even when individual traits show signs of recovery. Our results reveal that both physiological recovery and microbial community recovery are strongly shaped by the plant host species identity and drought duration This study widens knowledge of SF tropical forests, vulnerable habitats in the context of climate change, through the lens of the associated microbial communities and functional traits. Beyond the effects of an increasingly uncertain climate combined with a rise in the frequency of extreme events, our study places emphasis on including tree species extended phenotypes in considering their recovery dynamics. Graphical Abstract