Effects of monsoons and storms on the structuring and diversity of picoeukaryotic microbial communities in a tropical coastal environment

Abstract

Picoeukaryotes are key components in marine ecosystems that play crucial roles in food webs and biogeochemical cycles. Despite their significance, many aspects of their community ecology and diversity remain understudied. Here, we investigated the taxonomic and functional diversity of picoeukaryotic communities in response to monsoonal patterns and weather disturbances brought about by storms, characterizing tropical coastal regions. To do this, water samples were collected almost weekly or bi-weekly at a single location in a tropical coastal environment covering the late northeast (NE) and southwest (SW) monsoons. We then performed high-throughput amplicon sequencing of the V4 region of the 18S rRNA gene to generate taxonomic profiles of the communities across time. Clustering based on environmental parameters grouped our samples into months associated with NE monsoon, SW monsoon, and stormy SW monsoon, demonstrating seasonality influenced by monsoons and storms, typically observed in tropical coastal waters. In comparison, clustering based on abundance only grouped the samples into NE and SW monsoon, with most communities during storm period joining the NE monsoon samples. These samples exhibited greater diversity, with smaller taxa such as Syndiniales, Prymnesiophyceae, Picozoa, Cercozoa, Stramenopiles, and Chlorophytes being the most abundant groups present. In contrast, SW monsoon samples have lower diversity but have become generally dominated by large-celled taxa, mostly diatoms. Multivariate and correlation analyses both revealed nitrate as the strongest environmental driver of the picoeukaryotic community structuring. Meanwhile, network analysis grouped the taxa into three modules, more consistent with the clustering based on environmental parameters, implying that although storms may not significantly change the community composition, they may however influence the dominating taxa. Each module was composed of a unique set of co-occurring taxa, highlighting high turnover of picoeukaryotic communities between each season. In addition, our results showed that SW monsoon-associated module had higher interconnectivity than other modules, suggesting that the interactions during this period may be less species-specific, thus, more adaptable than during NE monsoon. However, we observed that extreme fluctuations caused by storms could have possibly allowed for selection of dominant taxa. Shotgun metagenomic sequencing of representative samples from each monsoon period also revealed that differently abundant functional genes, particularly genes associated to nitrogen metabolism, might have also helped in adaptation to the changing nutrient conditions. Our observations provide new insights on the potential trajectory of microbial communities under environmental stresses, which are important in understanding the implications of emerging threats such as coastal eutrophication and climate change.