Greater transmission capacities and small-world characteristics of bacterial communities in the above- than those in the below- ground niches of a typical submerged macrophyte, Vallisneria natans

Sci Total Environ. 2023 Dec 10:903:166229. doi: 10.1016/j.scitotenv.2023.166229. Epub 2023 Aug 14.

Abstract

Leaves and roots of submerged macrophytes provide extended surfaces and stable internal tissues for distinct microorganisms to rest, but how these microorganisms interact with each other across different niches and ultimately drive the distribution through horizontal and vertical transmissions remains largely undetermined. Knowledge of the mechanisms of assemblage and transmission in aquatic macrophytes-associated microbial communities will help to better understanding their important roles in plant fitness and benefit ecological functions. Here, we conducted a microcosmic experiment based on in situ lake samples to investigate the bacterial community assemblage, transmission, and co-occurrence patterns in different niches of a typical submerged macrophyte, Vallisneria natans (V. natans), including seed endosphere, as well as environmental (water and bulk sediment), epiphytic (phyllosphere and rhizosphere), and endophytic (leaf and root endosphere) microhabitats of both leaves and roots representatives of the above- and below- ground niches (AGNs and BGNs), respectively. We found the bacterial communities colonized in epiphytic niches not only exhibited the highest diversity compared to adjacent environmental and endophytic niches, but also dominated the interactions between those bacterial members of neighboring niches in both AGNs and BGNs. The host plants promoted niche specificity at bacterial community-level, as confirmed by the proportion of bacterial specialists increased with plant proximity, especially in the BGNs. Furthermore, the bacterial taxa colonized in the AGNs exhibited higher horizontal and vertical transmission capacities than those in the BGNs, especially in the vertical transmission from seeds to leaves (41.38 %) than roots (0.42 %). Meanwhile, the bacterial co-occurrence network in AGNs was shown to have stronger small-world characteristics but weaker stability than those in the BGNs. Overall, this study cast new light on the plant microbiome in the aquatic environment, thus better promoting the potential development of strategies for breeding aquatic macrophyte holobiont with enhanced water purification and pollutant removal capabilities in the future.

Keywords: Aquatic environment; Bacterial community assemblage; Bacterial transmission; Phyllosphere; Rhizosphere.