Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean

Abstract

Despite being the world’s third largest ocean, the Indian Ocean is one of the least studied and understood with respect to microbial diversity as well as biogeochemical and ecological functions. In this study, we investigated the microbial community and its metabolic potential for nitrogen (N) acquisition in the oligotrophic surface waters of the Indian Ocean using a metagenomic approach. Proteobacteria and Cyanobacteria dominated the microbial community with an average 37.85 and 23.56% of relative abundance, respectively, followed by Bacteroidetes (3.73%), Actinobacteria (1.69%), Firmicutes (0.76%), Verrucomicrobia (0.36%), and Planctomycetes (0.31%). Overall, only 24.3% of functional genes were common among all sampling stations indicating a high level of gene diversity. However, the presence of 82.6% common KEGG Orthology (KOs) in all samples showed high functional redundancy across the Indian Ocean. Temperature, phosphate, silicate and pH were important environmental factors regulating the microbial distribution in the Indian Ocean. The cyanobacterial genus Prochlorococcus was abundant with an average 17.4% of relative abundance in the surface waters, and while 54 Prochlorococcus genomes were detected, 53 were grouped mainly within HLII clade. In total, 179 of 234 Prochlorococcus sequences extracted from the global ocean dataset were clustered into HL clades and exhibited less divergence, but 55 sequences of LL clades presented more divergence exhibiting different branch length. The genes encoding enzymes related to ammonia metabolism, such as urease, glutamate dehydrogenase, ammonia transporter, and nitrilase presented higher abundances than the genes involved in inorganic N assimilation in both microbial community and metagenomic Prochlorococcus population. Furthermore, genes associated with dissimilatory nitrate reduction, denitrification, nitrogen fixation, nitrification and anammox were absent in metagenome Prochlorococcus population, i.e., nitrogenase and nitrate reductase. Notably, the de novo biosynthesis pathways of six different amino acids were incomplete in the metagenomic Prochlorococcus population and Prochlorococcus genomes, suggesting compensatory uptake of these amino acids from the environment. These results reveal the features of the taxonomic and functional structure of the Indian Ocean microbiome and their adaptive strategies to ambient N deficiency in the oligotrophic ocean.

Metabolic tuning of a stable microbial community in the surface oligotrophic Indian Ocean revealed by integrated meta-omics

“…Therefore, to minimize the uncertainty caused by the lack of replication, both metagenomic and metaproteomic analyses were conducted and the results show that the dominant taxa at site S8, Synechococcus, was responsible for most of the variation in microbial community composition. This observation is consistent with site S8 being close to the coast where Synechococcus is the usually the dominant cyanobacterial group (Karlusich et al 2020;Wang et al 2021). Interestingly, a recent study has shown that true replication is not always possible in oceanography, because the ocean is a fluid environment and 'replicate' samples from different water mass might actually be collected even within a short time (Saito et al 2019).…”

The synergistic effects of plants and nitrogen on microbial hitchhiking

“…Especially when plants have no membrane, cell motility and Bacillus of H2 are the highest compared with other plants. Nitrogen can trigger genes related to motility in motile bacteria and rewiring of the nitrogen regulation system(Karthikeyan et al, 2021; Kavamura et al, 2018; Sun et al, 2020; Wang et al, 2021; Zhou et al, 2017). At the same time, plant secretions were different under different concentrations.…”

“…Previous studies have suggested that root length and root surface area increased under intermediate N levels and that root growth was reduced under both higher and lower fertilization levels, affecting plant morphology(Chen et al, 2020; Good and Beatty, 2011). On the other hand, nitrogen is functional in the construction of and chlorophyll, which can influence plant growth and development by affecting photosynthesis and the uptake of minerals(Grossart et al, 2001; Kavamura et al, 2018; Razaq et al, 2017; Wang et al, 2021). In addition to these reasons, in our study, we found that in the treatment group with filter-membrane addition, there was no significant difference in the growth of spinach with different nitrogen concentrations.…”

“…Previous studies have suggested that root length and root surface area increased under intermediate N levels and that root growth was reduced under both higher and lower fertilization levels, affecting plant morphology Good and Beatty, 2011). On the other hand, nitrogen is functional in the construction of and chlorophyll, which can influence plant growth and development by affecting photosynthesis and the uptake of minerals (Grossart et al, 2001;Kavamura et al, 2018;Razaq et al, 2017;Wang et al, 2021).…”

Microbiome Studies from Saudi Arabia over the Last 10 Years: Achievements, Gaps, and Future Directions

“…Rhodanobacter and Rhodocyclaceae are sensors for the presence of uranium, and Oceanospirillales is a good indicator for oil contamination [ 36 ]. Metagenome-based analysis of microbial diversity and ecology of soil, river, lake, seashore, mangrove, ocean water and sediments could indicate the metabolic architecture of the specific microbiome and could also be a marker for water quality, various pollutants, and chemical contaminations [ 37 , 38 , 39 , 40 , 41 , 42 ] ( Table 1 ). Metagenome of water sediment can also be used for public health risk assessment [ 43 ].…”