Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents

Abstract

Little is known about evolutionary drivers of microbial populations in the warm subseafloor of deep-sea hydrothermal vents. Here we reconstruct 73 metagenome-assembled genomes (MAGs) from two geochemically distinct vent fields in the Mid-Cayman Rise to investigate patterns of genomic variation within subseafloor populations. Low-abundance populations with high intra-population diversity coexist alongside high-abundance populations with low genomic diversity, with taxonomic differences in patterns of genomic variation between the mafic Piccard and ultramafic Von Damm vent fields. Populations from Piccard are significantly enriched in nonsynonymous mutations, suggesting stronger purifying selection in Von Damm relative to Piccard. Comparison of nine Sulfurovum MAGs reveals two high-coverage, low-diversity MAGs from Piccard enriched in unique genes related to the cellular membrane, suggesting these populations were subject to distinct evolutionary pressures that may correlate with genes related to nutrient uptake, biofilm formation, or viral invasion. These results are consistent with distinct evolutionary histories between geochemically different vent fields, with implications for understanding evolutionary processes in subseafloor microbial populations.

Fig. 1

Relationships between SNV density, average majority allele frequency, and mean coverage for MAGs identified from the two vent fields. a Piccard vent field, b Von Damm vent field. Each bubble represents one MAG. Color of bubble indicates taxonomic assignment. Bubble size indicates average MAG coverage normalized to number of reads in metagenome. Bubble size references represent coverages of 10× and 1000× for a 100 million read metagenome

Fig. 2

Violin plots showing a kernel density estimation of the underlying distribution of the SAAV to SNV ratio for all MAGs from the Piccard (red) and Von Damm (blue) vent fields. The boxes inside each plot denote the upper and lower quartiles within the distribution, the white dot represents the average. Numbers below each violin indicate the number of MAGs included in that sample. a All MAGs from Piccard and Von Damm; b Thiotrichales MAGs only; c Methanococci MAGs only; d Sulfurovum MAGs only. Differences in the distribution of the logs of the SAAV/SNV ratio between MAGs from Piccard and Von Damm were significant for all MAGs (t-test, p: 0.0005) and for Thiotrichales (t-test, p: 0.0002)

Fig. 3

Relationships among Sulfurovum MAGs according to universal gene phylogeny, ANI, and gene content. a Phylogenetic tree based on concatenated single-copy universal marker proteins. Sulfurovum MAGs are indicated in light red (Piccard) and light blue (Von Damm); reference genomes have no color designation. b Heatmap and cluster dendrogram grouping MAGs according to ANI. c Hierarchical clustering dendrogram based the presence and absence of ORF clusters in MAGs. MAGs are colored according to vent field; red is Piccard, blue is Von Damm

Fig. 4

COG categories for all gene clusters that were unique to Sulfurovum MAGs. FS854_Bin37 and FS856_Bin99. COG categories that were significantly enriched relative to all genes in all Sulfurovum MAGs are indicated with asterisks