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

Abstract

Selection by the local, contemporary environment plays a prominent role in shaping the biogeography of microbes. However, the importance of historical factors in microbial biogeography is more debatable. Historical factors include past ecological and evolutionary circumstances that may have influenced present-day microbial diversity, such as dispersal and past environmental conditions. Diverse thermophilic sulfate-reducing Desulfotomaculum are present as dormant endospores in marine sediments worldwide where temperatures are too low to support their growth. Therefore, they are dispersed to here from elsewhere, presumably a hot, anoxic habitat. While dispersal through ocean currents must influence their distribution in cold marine sediments, it is not clear whether even earlier historical factors, related to the source habitat where these organisms were once active, also have an effect. We investigated whether these historical factors may have influenced the diversity and distribution of thermophilic endospores by comparing their diversity in 10 Arctic fjord surface sediments. Although community composition varied spatially, clear biogeographic patterns were only evident at a high level of taxonomic resolution (>97% sequence similarity of the 16S rRNA gene) achieved with oligotyping. In particular, the diversity and distribution of oligotypes differed for the two most prominent OTUs (defined using a standard 97% similarity cutoff). One OTU was dominated by a single ubiquitous oligotype, while the other OTU consisted of ten more spatially localized oligotypes that decreased in compositional similarity with geographic distance. These patterns are consistent with differences in historical factors that occurred when and where the taxa were once active, prior to sporulation. Further, the influence of history on biogeographic patterns was only revealed by analyzing microdiversity within OTUs, suggesting that populations within standard OTU-level groupings do not necessarily share a common ecological and evolutionary history.

Freezing Tolerance of Thermophilic Bacterial Endospores in Marine Sediments

“…DNA was extracted directly from the sediment following pretreatment at −80°C or −20°C, and from the +4°C unfrozen control (i.e., prior to pasteurization), from slurry subsamples before the +50°C incubation (i.e., immediately after pasteurization) and again after 7 days of incubation at +50°C. Assessing the community composition after 7 days is consistent with observations that this is a sufficient time frame for uncovering thermospore richness in heated sediment incubations (Chakraborty et al, 2018; Hanson et al, 2019). Procedural blank DNA extractions, i.e., without any subsample added, were performed in parallel with each batch of DNA extractions.…”

“…Previous studies have shown that thermospores from cold marine sediments germinate upon incubation at high temperature (Hubert et al, 2009, 2010; de Rezende et al, 2013; Müller et al, 2014; Volpi et al, 2017; Bell et al, 2018; Chakraborty et al, 2018; Hanson et al, 2019). In this study, as in previous studies, sulfate consumption at +50°C after pasteurization corresponded with an increase in the relative sequence abundance of putative sulfate-reducing bacteria.…”

“…Thermophilic endospore-forming bacteria (thermospores) have been discovered in cold marine sediments through conducting high-temperature (50°C) incubation experiments (Hubert et al, 2009; de Rezende et al, 2013; Müller et al, 2014; Volpi et al, 2017; Bell et al, 2018; Chakraborty et al, 2018; Hanson et al, 2019). These misplaced thermophiles are members of the dormant microbial seed bank and are conspicuously alien to these cold environments where they cannot grow and divide.…”

Biogeochemistry and microbiology of high Arctic marine sediment ecosystems—Case study of Svalbard fjords

“…Potential sources could be the abundant seep sites releasing thermogenic methane off southwest Spitsbergen (e.g., Lund Myhre et al 2016). Based on their inability to grow and multiply in cold ocean water and sediments, such thermospores are not subject to local environmental selection and may therefore be used as biogeographic tracers to show how microbial cells are passively dispersed with ocean currents in the Arctic (Müller et al 2014;Hanson et al 2019).…”

Exploring the microdiversity within marine bacterial taxa: Towards an integrated biogeography in the Southern Ocean

“…Initially, the consensus was that the rapid and widespread dispersal of microbes should erase any signal of past historical events [1]. Nevertheless, it is now clear that historical processes, such as the dispersal barriers and geographic distance, might substantially contribute to microbes’ biogeography instead of environmental filtering [5, 10, 11]. For instance, biogeographic regionalization, isolation, and endemism have been reported for microbes, as well as in larger organisms, and evidence a predominant effect of geographic distance over environmental variations [12, 13].…”