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

Marine-terrestrial colonization represents one of the most seminal transition in microbial ecology and evolution. Understanding the distribution and drivers of soil microbial communities in transient nascent ecosystems is critical giving the role of microbes in soil biogeochemistry and their multifaceted influence on ecosystem succession. Here we studied a well-established salt marsh chronosequence spanning over a century of ecosystem development and provide high-resolution patterns of fungal community composition, diversity and ecological succession through soil formation. Noteworthy, despite presenting 10- to 100-fold lowered fungal abundances, initial soil sites held comparable richness as observed for more mature soils. These initial sites also exhibited significant temporal variations in ß-diversity, which may be attributed to the great dynamics imposed by the tides. The fungal community compositions changed substantially along the succession, revealing a clear signature of ecological replacement by gradually decoupling the marine environment towards a terrestrial system. Fungal taxonomic distributions were further interpreted in the context of their ecophysiology and potential role in the ecosystem. Moreover, distance-based linear modelling revealed soil physical structure and organic matter to be the best predictors of the shifts in fungal ß-diversity along the chronosequence. Taken together, our study lays a basis of understanding of the spatiotemporally-determined fungal community dynamics in salt marsh soils and highlights their ecophysiological traits and adaptation in an evolving ecosystem.

海陆定植是微生物生态学与演化历程中最具里程碑意义的转型事件之一。鉴于微生物在土壤生物地球化学循环中的核心作用，以及其对生态系统演替的多维度影响，解析暂态新生生态系统中土壤微生物群落的分布格局与驱动因子至关重要。本研究依托一套已被充分验证的盐沼时间序列样带（该样带涵盖了超过百年的生态系统发育历程），系统解析了土壤形成过程中真菌群落组成、多样性及生态演替的高分辨率分布模式。值得注意的是，尽管初始土壤样点的真菌丰度较成熟土壤低10至100倍，但其物种丰富度却与成熟土壤相当。此类初始样点的β多样性（β-diversity）亦呈现显著的时间变异，这一现象可归因于潮汐作用带来的强烈环境动态变化。真菌群落组成随演替进程发生显著改变，呈现出清晰的生态替代特征——群落结构逐渐脱离海洋环境特征，向陆地生态系统方向转变。研究进一步结合真菌的生理生态特征及其在生态系统中的潜在功能，对其分类群分布格局进行了解析。此外，基于距离的线性模型分析表明，土壤物理结构与有机质含量是解释盐沼时间序列样带中真菌β多样性变化的最佳预测因子。综上，本研究为理解盐沼土壤中受时空格局调控的真菌群落动态提供了理论基础，并揭示了真菌在演化生态系统中的生理生态特征与适应策略。