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.

Highlights

  • Some microbes have globally widespread distributions while others do not; yet pinpointing the mechanisms responsible for these biogeographic patterns remains challenging (Hanson et al, 2012)

  • The role of historical factors in shaping the diversity and biogeography of microbes has been hotly debated for decades because – it is contended – microbes’ enormous potential for rapid and widespread dispersal should erase any signature of past events

  • Stations AB and EA lacked a second phase of sulfate reduction with concomitant butyrate and propionate consumption, suggesting that thermophilic sulfate-reducing bacteria (SRB) capable of utilizing these two organic acids were possibly absent from these stations or if present, did not grow; e.g., due to the absence of other bacteria

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Summary

Introduction

Some microbes have globally widespread distributions while others do not; yet pinpointing the mechanisms responsible for these biogeographic patterns remains challenging (Hanson et al, 2012). A classic perspective of biogeography divides the underlying mechanisms into two main categories: those that are driven by the contemporary, local environment versus those that rely on circumstances that have happened in the past (Martiny et al, 2006) These historical factors include all ecological and evolutionary events that previously influenced (either long ago or relatively recently) a present-day population or community, such as dispersal and past environmental conditions. Thermophilic, fermentative and sulfate-reducing endospore-forming bacteria within the phylum Firmicutes, including members of the genus Desulfotomaculum, are useful models for studying the role of historical factors in marine microbial biogeography These thermophiles are abundant in cold marine sediments as dormant endospores (Hubert et al, 2009; de Rezende et al, 2013; Volpi et al, 2017) and have been detected in marine sediments worldwide (Müller et al, 2014). Their distribution and diversity is the result of historical factors alone

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