Abstract
Oceanic microbial diversity covaries with physicochemical parameters. Temperature, for example, explains approximately half of global variation in surface taxonomic abundance. It is unknown, however, whether covariation patterns hold over narrower parameter gradients and spatial scales, and extending to mesopelagic depths. We collected and sequenced 45 epipelagic and mesopelagic microbial metagenomes on a meridional transect through the eastern Red Sea. We asked which environmental parameters explain the most variation in relative abundances of taxonomic groups, gene ortholog groups, and pathways—at a spatial scale of <2000 km, along narrow but well-defined latitudinal and depth-dependent gradients. We also asked how microbes are adapted to gradients and extremes in irradiance, temperature, salinity, and nutrients, examining the responses of individual gene ortholog groups to these parameters. Functional and taxonomic metrics were equally well explained (75–79%) by environmental parameters. However, only functional and not taxonomic covariation patterns were conserved when comparing with an intruding water mass with different physicochemical properties. Temperature explained the most variation in each metric, followed by nitrate, chlorophyll, phosphate, and salinity. That nitrate explained more variation than phosphate suggested nitrogen limitation, consistent with low surface N:P ratios. Covariation of gene ortholog groups with environmental parameters revealed patterns of functional adaptation to the challenging Red Sea environment: high irradiance, temperature, salinity, and low nutrients. Nutrient-acquisition gene ortholog groups were anti-correlated with concentrations of their respective nutrient species, recapturing trends previously observed across much larger distances and environmental gradients. This dataset of metagenomic covariation along densely sampled environmental gradients includes online data exploration supplements, serving as a community resource for marine microbial ecology.
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Acknowledgements
We thank chief scientist Amy Bower, co-chief scientist Yasser Abualnaja, Leah Trafford, Dan McCorkle and other scientists from the Woods Hole Oceanographic Institution, the captain and crew of the R/V Aegaeo and the Hellenic Center for Marine Research and Red Sea Research Center Director James Luyten for their help on the 2011 KAUST (King Abdullah University of Science and Technology) Red Sea Expedition. Assistance with DNA extraction was provided by Matt Cahill, David Ngugi and Francisco Acosta Espinosa. Bioinformatics assistance was provided by Mamoon Rashid and James Morton. Statistics assistance was provided by Mikyoung Jun, Myoungji Lee, Yoan Eynaud and James Morton. We thank Jon Sanders, Jenan Kharbush and Lihini Aluwihare for helpful comments on the manuscript. We also thank colleagues who suggested KOs hypothesized to have interesting ecological patterns: Paul Berube, Yue Guan, Laura Villanueva, Francisco Rodríguez-Valera, Nathan Ahlgren, Zhenfeng Liu, Francy Jiménez and Ulrike Pfreundt. This work was funded in part by a postdoctoral fellowship to LRT from the Saudi Basic Industries Corporation (SABIC).
Author contributions
LRT planned the study, organized the cruise, collected samples, curated physical and chemical data, extracted DNA, processed sequence data, generated graphics and tables and wrote the paper. GJW planned and executed statistical analyses and wrote the paper. MFH tested and ran taxonomic analyses and wrote the paper. AS collected samples and extracted DNA. PL ran metabolite prediction analysis. JS generated interactive visualizations. RK provided analytical input and wrote the paper. US planned the study, organized the cruise and wrote the paper.
Data Deposition
Sequence data have been submitted to the NCBI BioSample database with accession numbers PRJNA289734 (BioProject) and SRR2102994–SRR2103038 (SRA).
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Thompson, L., Williams, G., Haroon, M. et al. Metagenomic covariation along densely sampled environmental gradients in the Red Sea. ISME J 11, 138–151 (2017). https://doi.org/10.1038/ismej.2016.99
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DOI: https://doi.org/10.1038/ismej.2016.99
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