Trophic Selective Pressures Organize the Composition of Endolithic Microbial Communities From Global Deserts.

Evan B Qu,Chris R Omelon,Don A Cowan,Victoria Meslier,Jocelyne Diruggiero,Gillian Maggs-Kölling,Aharon Oren

doi:10.3389/fmicb.2019.02952

Abstract

Studies of microbial biogeography are often convoluted by extremely high diversity and differences in microenvironmental factors such as pH and nutrient availability. Desert endolithic (inside rock) communities are relatively simple ecosystems that can serve as a tractable model for investigating long-range biogeographic effects on microbial communities. We conducted a comprehensive survey of endolithic sandstones using high-throughput marker gene sequencing to characterize global patterns of diversity in endolithic microbial communities. We also tested a range of abiotic variables in order to investigate the factors that drive community assembly at various trophic levels. Macroclimate was found to be the primary driver of endolithic community composition, with the most striking difference witnessed between hot and polar deserts. This difference was largely attributable to the specialization of prokaryotic and eukaryotic primary producers to different climate conditions. On a regional scale, microclimate and properties of the rock substrate were found to influence community assembly, although to a lesser degree than global hot versus polar conditions. We found new evidence that the factors driving endolithic community assembly differ between trophic levels. While phototrophic taxa, mostly oxygenic photosynthesizers, were rigorously selected for among different sites, heterotrophic taxa were more cosmopolitan, suggesting that stochasticity plays a larger role in heterotroph assembly. This study is the first to uncover the global drivers of desert endolithic diversity using high-throughput sequencing. We demonstrate that phototrophs and heterotrophs in the endolithic community assemble under different stochastic and deterministic influences, emphasizing the need for studies of microorganisms in context of their functional niche in the community.

Highlights

Arid and hyper-arid regions of Earth pose a significant challenge to life, with stresses such as high solar radiation, sparse and intermittent rain events, and drastic temperature fluctuations exerting strong selective pressures on organisms (Potts and Webb, 1994; Lebre et al, 2017)
Archaea have been poorly reported in endolithic communities to the point where their presence is questioned (Pointing et al, 2009; Meslier et al, 2018); we found archaeal signatures in every site except University Valley, indicating that Archaea do contribute to the sandstone endolithic community, albeit at very low relative abundances
We suggest that complex assembly processes may be more discernible in the endolithic system because the assembly of these communities is influenced by more tractable environmental variables; the endolithic system may prove promising for further investigations of microbial biogeography

Summary

Introduction

Arid and hyper-arid regions of Earth pose a significant challenge to life, with stresses such as high solar radiation, sparse and intermittent rain events, and drastic temperature fluctuations exerting strong selective pressures on organisms (Potts and Webb, 1994; Lebre et al, 2017). Endolithic communities, which inhabit pore and fissure space within the interior of rocks, are perhaps the most xerotolerant of these microbial refuges, appearing in the driest environments on Earth such as the hyper-arid core of the Chilean Atacama Desert and the McMurdo Dry Valleys in Antarctica (Friedmann and Ocampo, 1976; Azua-Bustos et al, 2012) These communities usually colonize a thin layer underneath the surface of the rock and have been described in diverse substrates including sandstone (Friedmann et al, 1967; Walker and Pace, 2007), limestone (Wong et al, 2010), halite (de los Ríos et al, 2010), gypsum (DiRuggiero et al, 2013), ignimbrite (Wierzchos et al, 2013), and granite (de los Ríos et al, 2005). Diverse heterotrophic bacteria are found in the endolithic community, with the phyla Actinobacteria, Proteobacteria, Chloroflexi, Bacteroidetes, and Deinococcus-Thermus represented (Walker and Pace, 2007; Meslier et al, 2018; Wierzchos et al, 2018)

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