Predicting the response of the deep-ocean microbiome to geochemical perturbations by hydrothermal vents

Abstract

Submarine hydrothermal vents perturb the deep-ocean microbiome by injecting reduced chemical species into the water column that act as an energy source for chemosynthetic organisms. These systems thus provide excellent natural laboratories for studying the response of microbial communities to shifts in marine geochemistry. The present study explores the processes that regulate coupled microbial-geochemical dynamics in hydrothermal plumes by means of a novel mathematical model, which combines thermodynamics, growth and reaction kinetics, and transport processes derived from a fluid dynamics model. Simulations of a plume located in the ABE vent field of the Lau basin were able to reproduce metagenomic observations well and demonstrated that the magnitude of primary production and rate of autotrophic growth are largely regulated by the energetics of metabolisms and the availability of electron donors, as opposed to kinetic parameters. Ambient seawater was the dominant source of microbes to the plume and sulphur oxidisers constituted almost 90% of the modelled community in the neutrally-buoyant plume. Data from drifters deployed in the region allowed the different time scales of metabolisms to be cast in a spatial context, which demonstrated spatial succession in the microbial community. While growth was shown to occur over distances of tens of kilometers, microbes persisted over hundreds of kilometers. Given that high-temperature hydrothermal systems are found less than 100 km apart on average, plumes may act as important vectors between different vent fields and other environments that are hospitable to similar organisms, such as oil spills and oxygen minimum zones.

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

“…These results are consistent with a gene-centric mathematical model of the Abe vent at ELSC, which shows that sulfur metabolisms dominate and that seafloor populations were rapidly diluted out of the rising plume (Reed et al, 2015) and also with more extensive analysis of ELSC plumes, showing that differences in community composition between vent fields are not significant (Sheik et al, 2015). Observed variation in the abundance of specific genes across specific samples is to be expected given the dynamic nature of plumes, and could reflect variation in the proportions of different water sources (end-member hydrothermal fluid, plume and background), which is a key determinant of plume community structure (Reed et al, 2015). Some consistent differences in the membership of dominant organisms were observed between vent fields, chiefly the increased abundance of Alteromonas and Marinobacter populations at Mariner (Sheik et al, 2015; Figure 2).…”

Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone

“…This "mass effect" (61) means that geochemical or biochemical information is needed to assign actual activity to genes or pathways identified in multiomic data, especially for components mediating energy metabolism. This conclusion is generalizable and should be applied to other ecosystems exhibiting dispersal across strong environmental gradients, such as estuaries (62) or hydrothermal vents (6). Moreover, in dynamic ecosystems with rapidly changing geochemical conditions, past population growth rates can influence future community structure and biomolecular patterns, and hence cross-sectional community profiles may not reflect current dynamics (63).…”

“…Metabolic flexibility encoded in the genomes of microorganisms mediating these processes may also contribute to broader distributions of individual genes than their predicted activity range (30). This disconnect between local metabolic potential and activity needs to be considered when interpreting metagenomic profiles in a functional context, especially in environments with strong redox gradients, such as OMZs (9) or hydrothermal vents (6).…”

“…According to the central dogma of molecular biology (4), gene transcription and translation are intermediate steps that regulate metabolic processes in individual cells, but the appropriate projection of the central dogma to ecosystem scales remained unresolved, because transcription and translation were not explicitly considered in previous models (5,6). We have developed a biogeochemical model that explicitly incorporates multiomic sequence information and predicts pathway expression and growth in relation to geochemical conditions.…”

“…Recent work based on metagenomics and quantitative PCR (qPCR) suggests that biogeochemical processes may be described by models focusing on the population dynamics of individual genes (5,6). In such gene-centric models, genes are used as proxies for particular metabolic pathways, with gene production rates being determined solely by the Gibbs free energy Significance Modern molecular sequencing is beginning to provide great insight into microbial community structure and function at ecosystem scales.…”