Gulf of Mexico blue hole harbors high levels of novel microbial lineages

N. V. Patin^1,2,9,10,11, Z. A. Dietrich³, A. Stancil⁴, M. Quinan⁴, J. S. Beckler⁴, E. R. Hall⁵, J. Culter⁵, C. G. Smith⁶, M. Taillefert⁷, F. J. Stewart^1,2,8

Affiliations: ¹School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA; ²Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, GA, USA; ³Bowdoin College, Brunswick, ME, USA; ⁴ Harbor Branch Oceanographic Institute, Florida Atlantic University, Ft. Pierce, FL, USA; ⁵ Mote Marine Laboratory, Sarasota, FL, USA; ⁶ U.S. Geological Survey, St. Petersburg Coastal and Marine Science Center, St. Petersburg, FL, USA

Abstract

Exploration of oxygen-depleted marine environments has consistently revealed novel microbial taxa and metabolic capabilities that expand our understanding of microbial evolution and ecology. Marine blue holes are shallow karst formations characterized by low oxygen and high organic matter content. They are logistically challenging to sample, and thus our understanding of their biogeochemistry and microbial ecology is limited. We present a metagenomic and geochemical characterization of Amberjack Hole on the Florida continental shelf (Gulf of Mexico). Dissolved oxygen became depleted at the hole’s rim (32 m water depth), remained low but detectable in an intermediate hypoxic zone (40–75 m), and then increased to a secondary peak before falling below detection in the bottom layer (80–110 m), concomitant with increases in nutrients, dissolved iron, and a series of sequentially more reduced sulfur species. Microbial communities in the bottom layer contained heretofore undocumented levels of the recently discovered phylum Woesearchaeota (up to 58% of the community), along with lineages in the bacterial Candidate Phyla Radiation (CPR). Thirty-one high-quality metagenome-assembled genomes (MAGs) showed extensive biochemical capabilities for sulfur and nitrogen cycling, as well as for resisting and respiring arsenic. One uncharacterized gene associated with a CPR lineage differentiated hypoxic from anoxic zone communities. Overall, microbial communities and geochemical profiles were stable across two sampling dates in the spring and fall of 2019. The blue hole habitat is a natural marine laboratory that provides opportunities for sampling taxa with under-characterized but potentially important roles in redox-stratified microbial processes.

Cite the article: Patin, N.V., Dietrich, Z.A., Stancil, A. et al. Gulf of Mexico blue hole harbors high levels of novel microbial lineages. ISME J (2021). https://doi.org/10.1038/s41396-021-00917-x

Metagenome Sequence Data and MAGs Narrative

This Narrative contains the metagenomic sequence data from the paper. The data files can be accessed through Figshare at https://figshare.com/projects/Amberjack_Blue_Hole/85013. The metagenomes are found in the PairedEndLibrary objects. The shotgun metagenome for September 2019 at 95 M is titled BH091995M_S2_L001_R2_001.fastq.gz_reads, for September 2019 at 60 M titled BH091960M_S1_L001_R1_001.fastq.gz, for May 2019 at 106 M titled BH-51_S2_L001_R2_001.fastq.gz_reads, and May 2019 at 60 M titled BH-37_S1_L001_R1_001.fastq.gz_reads.

The metagenome-assembled genomes can be found in the assemblies, and all the assemblies are grouped together in the AssemblySet titled BH_MAGs. For a more detailed explanation of the MAGs, please see Table 1 of the associated publication. Most of the MAG assembly objects in this Narrative end with a numerical identifier corresponding to an entry on that table. The assembly Nitrosopumilus_manual__ corresponds to MAG BH19 in that table.

The Nitrosopumilus_manual assembly was manually binned, and the assemblies with _ed in the name were manually edited post-binning. Detail can be found in the Methods section of the manuscript under the heading "Manual MAG refinement and generation."

If you use these data, please cite them. Data citations can be found at the Figshare page linked above or downloaded directly here.