Distribution of thermophilic endospores in a temperate estuary indicate that dispersal history structures sediment microbial communities

Abstract

Endospores of thermophilic bacteria are found in cold and temperate sediments where they persist in a dormant state. As inactive endospores that cannot grow at the low ambient temperatures, they are akin to tracer particles in cold sediments, unaffected by factors normally governing microbial biogeography (e.g., selection, drift, mutation). This makes thermophilic endospores ideal model organisms for studying microbial biogeography since their spatial distribution can be directly related to their dispersal history. To assess dispersal histories of estuarine bacteria, thermophilic endospores were enriched from sediments along a freshwater-to-marine transect of the River Tyne in high temperature incubations (50°C). Dispersal histories for 75 different taxa indicated that the majority of estuarine endospores were of terrestrial origin; most closely related to bacteria from warm habitats associated with industrial activity. A subset of the taxa detected were marine derived, with close relatives from hot deep marine biosphere habitats. These patterns are consistent with the sources of sediment in the River Tyne being predominantly terrestrial in origin. The results point to microbial communities in estuarine and marine sediments being structured by bi-directional currents, terrestrial run-off and industrial effluent as vectors of passive dispersal and immigration.

Historical Factors Associated With Past Environments Influence the Biogeography of Thermophilic Endospores in Arctic Marine Sediments

“…Additionally, the diversity of thermophilic endospores in a single cold sediment can be considerable (de Rezende et al, 2013; Müller et al, 2014; Chakraborty et al, 2018) and may be explained by different taxa originating from different warm sources. These biogeographic studies also show that, despite being well-equipped for long-distance dispersal as spores, dispersal limitation influences the biogeography of some thermophilic endospores, while others are more cosmopolitan in distribution (Müller et al, 2014; Bell et al, 2018; Chakraborty et al, 2018). For example, Müller et al (2014) detected 146 unique phylotypes (i.e., OTUs with ≥97% 16S rRNA sequence identity) in a global survey of over 80 sediments, with some phylotypes present across many geographically distant locations and others detected in only a few samples.…”

“…Several studies have specifically investigated dispersal of thermophilic endospores by characterizing their biogeographic distribution in marine sediments at regional scales (de Rezende et al, 2013; Chakraborty et al, 2018) and global scales (Müller et al, 2014) as well as in estuarine systems (Bell et al, 2018). These studies have provided growing evidence in support of the hypothesis that many thermophilic endospores are derived from fluid flow expelled from marine deep biosphere ecosystems such as mid-ocean ridge venting systems and deeply buried hydrocarbon reservoirs, and are subsequently deposited to marine sediments via passive dispersal.…”

Contrasting community composition of endospores and vegetative Firmicutes in a marine sediment suggests both endogenous and exogenous sources of endospore accumulation

“…The limited ability of such conventional procedures to recover endospore DNA from environmental samples was also documented in studies of the presence of thermophilic endospores in marine sediments (Müller et al, ; de Rezende et al, 2013; Bell et al . ) and by endospore spike‐in tests (Dineen et al, ). Although we cannot exclude the possibility of endospore DNA co‐extraction in the conventional DNA extracts, we conclude that such possible co‐extraction has a minor influence on our data.…”

An Unexpectedly Broad Thermal and Salinity-Tolerant Estuarine Methanogen Community

“…that dominated an enrichment culture from a high-temperature oil field water production [ 39 ] ( Figure 4 ) after transport and 4 °C storage for months demonstrated that at least some remain viable following inactivity at low temperatures. Regardless, the short lag phases observed in the current study (<48 h) suggest constant replenishment of Methanothermobacter into the Tyne estuary sediment, from terrestrial or marine sources, e.g., landfill, hot geological, industrial, or agricultural habitats [ 40 ]. Given the likely passive dispersal from these sources [ 41 , 42 ], we attempted to resolve their mesophilic and thermophilic origins by determining salinity tolerances as a secondary niche dimension ( Figure 5 A).…”