Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments.

BACKGROUND: Mangrove wetlands are coastal ecosystems with important ecological features and provide habitats for diverse microorganisms with key roles in nutrient and biogeochemical cycling. However, the overall metabolic potentials and ecological roles of microbial community in mangrove sediment are remained unanswered. In current study, the microbial and metabolic profiles of prokaryotic and fungal communities in mangrove sediments were investigated using metagenomic analysis based on PacBio single-molecule real time (SMRT) and Illumina sequencing techniques. RESULTS: Comparing to Illumina short reads, the incorporation of PacBio long reads significantly contributed to more contiguous assemblies, yielded more than doubled high-quality metagenome-assembled genomes (MAGs), and improved the novelty of the MAGs. Further metabolic reconstruction for recovered MAGs showed that prokaryotes potentially played an essential role in carbon cycling in mangrove sediment, displaying versatile metabolic potential for degrading organic carbons, fermentation, autotrophy, and carbon fixation. Mangrove fungi also functioned as a player in carbon cycling, potentially involved in the degradation of various carbohydrate and peptide substrates. Notably, a new candidate bacterial phylum named as Candidatus Cosmopoliota with a ubiquitous distribution is proposed. Genomic analysis revealed that this new phylum is capable of utilizing various types of organic substrates, anaerobic fermentation, and carbon fixation with the Wood-Ljungdahl (WL) pathway and the reverse tricarboxylic acid (rTCA) cycle. CONCLUSIONS: The study not only highlights the advantages of HiSeq-PacBio Hybrid assembly for a more complete profiling of environmental microbiomes but also expands our understanding of the microbial diversity and potential roles of distinct microbial groups in biogeochemical cycling in mangrove sediment. Video Abstract.

Biogeography, Assembly Patterns, Driving Factors, and Interactions of Archaeal Community in Mangrove Sediments.

Archaea are a major part of Earth's life. They are believed to play important roles in nutrient biogeochemical cycling in the mangrove. However, only a few studies on the archaeal community in mangroves have been reported. In particular, the assembly processes and interaction patterns that impact the archaeal communities in mangroves have not been investigated to date. Here, the biogeography, assembly patterns, and driving factors of archaeal communities in seven representative mangroves across southeastern China were systematically analyzed. The analysis revealed that the archaeal community is more diverse in surface sediments than in subsurface sediments, and more diverse in mangroves at low latitudes than at high latitudes, with Woesearchaeota and Bathyarchaeota as the most diverse and most abundant phyla, respectively. Beta nearest-taxon index analysis suggested a determinant role of homogeneous selection on the overall archaeon community in all mangroves and in each individual mangrove. In addition, the conditionally rare taxon community was strongly shaped by homogeneous selection, while stochastic processes shaped the dominant taxon and always-rare taxon communities. Further, a moderate effect of environmental selection on the archaeal community was noted, with the smallest effect on the always-rare taxon community. Mangrove location, mean annual temperature, and salinity were the major factors that greatly affected the community composition. Finally, network analysis revealed comprehensive cooccurrence relationships in the archaeal community, with a crucial role of Bathyarchaeota. This study expands the understanding of the biogeography, assembly patterns, driving factors, and cooccurrence relationships of the mangrove archaeal community and inspires functional exploration of archaeal resources in mangrove sediments. IMPORTANCE As a key microbial community component with important ecological roles, archaea merit the attention of biologists and ecologists. The mechanisms controlling microbial community diversity, composition, and biogeography are central to microbial ecology but poorly understood. Mangroves are located at the land-ocean interface and are an ideal environment for examining the above questions. We here provided the first-ever overview of archaeal community structure and biogeography in mangroves located along an over-9,000-km coastline of southeastern China. We observed that archaeal diversity in low-latitude mangroves was higher than that in high-latitude mangroves. Furthermore, our data indicated that homogeneous selection strongly controlled the assembly of the overall and conditionally rare taxon communities in mangrove sediments, while the dominant taxon and always-rare taxon communities were mainly controlled by dispersal limitation.

High-Level Diversity of Basal Fungal Lineages and the Control of Fungal Community Assembly by Stochastic Processes in Mangrove Sediments.

Fungi are key components of microbial communities in mangrove wetlands, with important roles in the transformation of nutrients and energy. However, existing studies typically focus on cultivable fungi and seldom on the structure and driving factors of entire fungal communities. The compositions, community assembly, and interaction patterns of mangrove fungal communities on a large scale remain elusive. Here, biogeography, assembly, and co-occurrence patterns of fungal communities in mangroves across eastern to southern China were systematically analyzed by targeting the entire internal transcribed spacer (ITS) region with high-throughput Pacific Biosciences single-molecule real-time sequencing. The analysis revealed a high level of fungal diversity, including a number of basal fungal lineages not previously reported in mangroves, such as Rozellomycota and Chytridiomycota. Beta nearest-taxon index analyses suggested a determinant role of dispersal limitation on fungal community in overall and most individual mangroves, with support from the strong distance-decay patterns of community similarity. Further, nonmetric multidimensional scaling analyses revealed similar biogeographies of dominant and rare fungal communities. A minor role of environmental selection on the fungal community was noted, with geographical location and sediment depth as crucial factors driving the distribution of both, the dominant and rare taxa. Finally, network analysis revealed high modularized co-occurrence patterns of fungal community in mangrove sediments, and the keystone taxa might play important roles in microbial interactions and ecological functions. The investigation expands our understanding of biogeography, assembly patterns, driving factors, and co-occurrence relationships of mangrove fungi and will spur the further functional exploration and protection of fungal resources in mangroves. IMPORTANCE As key components of microbial community in mangroves, fungi have important ecological functions. However, the fungal community in mangroves on a large scale is generally elusive, and mangroves are declining rapidly due to climate change and anthropogenic activities. This work provides an overview of fungal community structure and biogeography in mangrove wetlands along a >9,000-km coastline across eastern to southern China. Our study observed a high number of basal fungal lineages, such as Rozellomycota and Chytridiomycota, in mangrove sediments. In addition, our results highlight a crucial role of dispersal limitation and a minor role of environmental selections on fungal communities in mangrove sediments. These novel findings add important knowledge about the structure, assembly processes, and driving factors of fungal communities in mangrove sediments.