Ecological succession reveals potential signatures of marine–terrestrial transition in salt marsh fungal communities

Abstract

Marine-to-terrestrial transition represents one of the most fundamental shifts in microbial life. Understanding the distribution and drivers of soil microbial communities across coastal ecosystems is critical given the roles of microbes in soil biogeochemistry and their multifaceted influence on landscape succession. Here, we studied the fungal community dynamics in a well-established salt marsh chronosequence that spans over a century of ecosystem development. We focussed on providing high-resolution assessments of community composition, diversity and ecophysiological shifts that yielded patterns of ecological succession through soil formation. Notably, despite containing 10-to 100-fold lower fungal internal transcribed spacer abundances, early-successional sites revealed fungal richnesses comparable to those of more mature soils. These newly formed sites also exhibited significant temporal variations in β-diversity that may be attributed to the highly dynamic nature of the system imposed by the tidal regime. The fungal community compositions and ecophysiological assignments changed substantially along the successional gradient, revealing a clear signature of ecological replacement and gradually transforming the environment from a marine into a terrestrial system. Moreover, distance-based linear modelling revealed soil physical structure and organic matter to be the best predictors of the shifts in fungal β-diversity along the chronosequence. Taken together, our study lays the basis for a better understanding of the spatiotemporally determined fungal community dynamics in salt marshes and highlights their ecophysiological traits and adaptation in an evolving ecosystem.

Changes in soil microbial community structure during long‐term secondary succession

“…The bacterial and fungal absolute abundance, as indicated by gene copies, increased with succession years in the early stage (Figure ), which could be related to the gradual increase in soil nutrients and the fact that the high level of organic matter supplied enough carbon, nitrogen and energy sources for microbial growth (Jia, Cao, Wang, & Wang, ). These results are consistent with Dini‐Andreote et al (), who observed that ITS gene copy number increased along succession in salt marshes. However, the bacterial and fungal absolute abundances become stable after S3 (110 years), which is consistent with the results of Darcy et al ().…”

“…For example, Zhou et al () showed that in forest ecosystems, bacteria and fungi tended to dominate in the early and late successional stages, respectively, whereas Li et al () reported that fungal abundance was higher at the beginning of secondary succession in semi‐arid grassland ecosystems. Additionally, a clear directional shift was observed in fungal communities across successional stages in recently glacier soils with a primary succession gradient (Blaalid et al, ; Brown & Jumpponen, ), but no such shift was observed in marine–terrestrial ecosystems (Dini‐Andreote, Pylro, Baldrian, van Elsas, & Salles, ).…”

Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon

“…Fungi in freshwater ecosystems are stimulated by the availability of organic matter, particularly plant-derived detritus such as leaves, which plays an important first step in the degradation of terrestrial organic matter (Gessner and Schwoerbel, 1991;Nikolcheva et al, 2003;Grossart and Rojas-Jimenez, 2016;Fabian et al, 2017). The mycobenthos are also ubiquitous in shallow water marine sediments in coastal ecosystems (Newell et al, 1989;Newell, 1994;Gessner et al, 1997;Mohamed and Martiny, 2011;Dini-Andreote et al, 2016). However, it is poorly understood how the mycobenthos react to changing environmental conditions in estuarine habitats, where there is an annual flux of organic matter amounting tõ 0.5 Pg C (Hedges et al, 1997;Benner, 2004).…”

Cryptogams signify key transitions of bacteria and fungi in Arctic sand dune succession

“…In very young soils, richness is often low and then increases and stabilises or even decreases in later stages (Jackson, ; Nemergut et al , ; Fierer et al , ; Williams et al , ; Jiang et al , ). Primary succession gradients in which both bacteria and fungi have been studied show conflicting patterns with each other but generally agree on different trajectories for bacterial and fungal richness (Brown & Jumpponen, ; Cutler, et al , ; Dini‐Andreote, et al , ; Dini‐Andreote, et al , ; Jiang, et al , ). In our case, fungal richness remained rather stable under vegetation covered stages, while bacterial richness had a unimodal response.…”