Geological processes mediate a microbial dispersal loop in the deep biosphere

Abstract

The deep biosphere is the largest microbial habitat on Earth and features abundant bacterial endospores. Whereas dormancy and survival at theoretical energy minima are hallmarks of microbial physiology in the subsurface, ecological processes such as dispersal and selection in the deep biosphere remain poorly understood. We investigated the biogeography of dispersing bacteria in the deep sea where upward hydrocarbon seepage was confirmed by acoustic imagery and geochemistry. Thermophilic endospores in the permanently cold seabed correlated with underlying seep conduits reveal geofluid-facilitated cell migration pathways originating in deep petroleum-bearing sediments. Endospore genomes highlight adaptations to life in anoxic petroleum systems and bear close resemblance to oil reservoir microbiomes globally. Upon transport out of the subsurface, viable thermophilic endospores reenter the geosphere by sediment burial, enabling germination and environmental selection at depth where new petroleum systems establish. This microbial dispersal loop circulates living biomass in and out of the deep biosphere.

Environmental selection influences the microbiome of subsurface petroleum reservoirs

“…Heuer et al (2020) postulated that vegetative cells and endospores that are deposited in surface sediments and undergo burial over geological timescales can then be revived under the right selective conditions. This is consistent with recent observations in a 1,180 m sediment core sampled during IODP Expedition 370 (Beulig et al 2022), and the concept of a microbial dispersal loop proposed for understanding the interplay of ecological principles of selection and migration in the subsurface (Mestre and Höfer et al 2020;Gittins et al 2022). Aside from geological processes such as sedimentation and petroleum fluid migration, natural dispersal vectors in the deep biosphere are limited (Stetter et al 1993).…”

“…2022), and the concept of a microbial dispersal loop proposed for understanding the interplay of ecological principles of selection and migration in the subsurface (Mestre and Höfer et al . 2020; Gittins et al . 2022).…”

Microbial diversity gradients in the geothermal mud volcano underlying the hypersaline Urania Basin

“…The mud volcano fluids and subsurface sediment microbial communities resemble each other in the presence of gram-positive, sometimes thermophilic, and presumably spore-forming genera and families within the phylum Firmicutes. Thus, the Urania Basin sediment microbiota provide an illustrative example for a “firmicute hotspot,” the previously postulated point sources that distribute endospore-forming, moderately thermophilic Firmicutes across cold marine sediments world-wide ( Hubert et al, 2009 ; Müller et al, 2014 ; Gittins et al, 2022 ). These spore-forming bacteria require a certain minimum temperature but cannot grow in deep-sea surficial sediments that are permanently cold.…”

Global biogeography of the smallest plankton across ocean depths

“…This mechanism has been shown to affect metacommunity structure by dampening distance-decay relationships and maintaining local diversity (69, 74, 75). Many prokaryotes reach the deep ocean from the surface through vertical dispersal (76) or disperse as endospores from sediments (77). However, DNA-based community composition data includes non-active bacterial cells (78), likely in dormancy state, to survive the very different conditions of the dark and cold deep ocean (77).…”

“…Many prokaryotes reach the deep ocean from the surface through vertical dispersal (76) or disperse as endospores from sediments (77). However, DNA-based community composition data includes non-active bacterial cells (78), likely in dormancy state, to survive the very different conditions of the dark and cold deep ocean (77). Therefore, a relatively higher proportion of dormant bacteria can create an apparent ‘homogenization’ of prokaryotic communities in deep zones.…”