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Trophic Selective Pressures Organize the Composition of Endolithic

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Trophic Selective Pressures Organize the Composition of Endolithic bioRxiv preprint doi: https://doi.org/10.1101/761262; this version posted September 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Trophic Selective Pressures Organize the Composition of 2 Endolithic Microbial Communities from Global Deserts 3 4 Evan Qu1, Chris Omelon2, Aharon Oren3, Victoria Meslier1, Don A. Cowan4, Gillian 5 Maggs-Kölling5, and Jocelyne DiRuggiero1§ 6 7 1Johns Hopkins University, Department of Biology, Baltimore, USA 8 2McGill University, Department of Biology, Montreal, Quebec Canada 9 3The Hebrew University of Jerusalem, Institute of Life Sciences, Edmond J. Safra 10 Campus, Jerusalem, Israel 11 4Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and 12 Microbiology, University of Pretoria, Pretoria, South Africa 13 5Gobabeb-Namib Research Institute, Walvis Bay, Namibia 14 15 §Correspondence: 16 Jocelyne DiRuggiero 17 [email protected] 18 Johns Hopkins University 19 Department of Biology 20 3400 N. Charles Street, Mudd Hall 235 21 Baltimore MD 21218, USA 1 bioRxiv preprint doi: https://doi.org/10.1101/761262; this version posted September 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 22 Abstract 23 Studies of microbial biogeography are often convoluted by extremely high diversity and 24 differences in microenvironmental factors such as pH and nutrient availability. Desert 25 endolithic (inside rock) communities are exceptionally simple ecosystems that can serve 26 as a tractable model for investigating long-range biogeographic effects on microbial 27 communities. We conducted a comprehensive survey of endolithic sandstones using 28 high-throughput marker gene sequencing to characterize global patterns of diversity in 29 endolithic microbial communities. We also tested a range of abiotic variables in order to 30 investigate the factors that drive community assembly at various trophic levels. 31 Macroclimate was found to be the primary driver of endolithic community composition, 32 with the most striking difference witnessed between hot and polar deserts. This difference 33 was largely attributable to the specialization of prokaryotic and eukaryotic primary 34 producers to different climate conditions. On a regional scale, microclimate and 35 properties of the rock substrate were found to influence community assembly, although to 36 a lesser degree than global hot versus polar conditions. We found new evidence that the 37 factors driving endolithic community assembly differ between trophic levels. While 38 phototrophic taxa were rigorously selected for among different sites, heterotrophic taxa 39 were more cosmopolitan, suggesting that stochasticity plays a larger role in heterotroph 40 assembly. This study is the first to uncover the global drivers of desert endolithic 41 diversity using high-throughput sequencing. We demonstrate that phototrophs and 42 heterotrophs in the endolithic community assemble under different stochastic and 43 deterministic influences, emphasizing the need for studies of microorganisms in context 44 of their functional niche in the community. 45 46 Keywords: endolithic, desert, xerotolerant, biogeography, trophic level, microbial 47 assembly 48 2 bioRxiv preprint doi: https://doi.org/10.1101/761262; this version posted September 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 49 Introduction 50 Arid and hyper-arid regions of Earth pose a significant challenge to life, with 51 stresses such as high solar radiation, sparse and intermittent rain events, and drastic 52 temperature fluctuations exerting strong selective pressures on organisms (Lebre et al., 53 2017; Potts and Webb, 1994). As aridity increases in an area and the diversity of higher 54 eukaryotic life decreases, microorganisms begin to constitute a larger component of the 55 total biomass and provide essential ecosystem functions such as carbon fixation and 56 biogeochemical cycling (Makhalanyane et al., 2015; Pointing and Belnap, 2012). Desert 57 microorganisms colonize rock and soil matrix as an adaptation to the harsh environmental 58 conditions, forming a category of microbial refuges that includes biological soil crusts, 59 hypoliths (under rock), epiliths (above rock), and endoliths (within rock) (Pointing and 60 Belnap, 2012). 61 Endolithic communities, which inhabit pore and fissure space within the interior 62 of rocks, are perhaps the most xerotolerant of these microbial refuges, appearing in the 63 driest environments on Earth such as the hyper-arid core of the Chilean Atacama Desert 64 and the McMurdo Dry Valleys in Antarctica (Azua-Bustos et al., 2012; Friedmann and 65 Ocampo, 1976). These communities usually colonize a thin layer underneath the surface 66 of the rock and have been described in diverse substrates including sandstone (Friedmann 67 et al., 1967; Walker and Pace, 2007), limestone (Wong et al., 2010), halite (de los Ríos et 68 al., 2010), gypsum (DiRuggiero et al., 2013), ignimbrite (Wierzchos et al., 2013), and 69 granite (de los Ríos et al., 2005). Depending on the nature of the substrate, the primary 70 mode of community colonization can either be cryptoendolithic, inhabiting pores within 71 the rock matrix or chasmoendolithic, inhabiting cracks and fissure space in the rocks 72 (Golubic et al., 1981). Within these communities, a few core photoautotrophic taxa along 73 with a variety of chemoheterotrophic taxa are found living in consortium. Cyanobacteria 74 are typically the dominant phototroph, often belonging to the multi-resistant genus 75 Chroococcidiopsis (Friedmann et al., 1967; Meslier et al., 2018; Wierzchos et al., 2018), 76 although eukaryotic green algae have also been reported in sandstone communities 77 (Walker and Pace, 2007), gypsum (Wierzchos et al., 2015) and halite communities from 78 the Atacama Desert (Robinson et al., 2015). Diverse heterotrophic bacteria are found in 79 the endolithic community, with the phyla Actinobacteria, Proteobacteria, Chloroflexi, 80 Bacteroidetes, and Deinococcus-Thermus particularly represented (Meslier et al., 2018; 81 Walker and Pace, 2007; Wierzchos et al., 2018). 82 Desert lithic habitats have been well-utilized for studies of microbial 83 biogeography, as their low diversity, simple trophic structure, and similar 84 microenvironment provides a tractable model when investigating spatial patterns in 85 microbial community assembly (Caruso et al., 2011). These studies have found that 86 environmental determinants, in particular climate, are the primary factors that organize 87 microbial communities at a global and regional scale (Chan et al., 2012; Friedmann, 88 1980; Lacap-Bugler et al., 2017). Biotic interactions are also thought to influence 89 community assembly, and endolithic Cyanobacteria have been reported to play a key role 90 in determining overall community structure and function (Valverde et al., 2015). 91 Conversely, it remains poorly understood how stochastic processes influence assembly 92 within the lithic habitat. Early studies of endolithic sandstones found remarkably similar 93 communities at global scales, which led to the hypothesis that these communities are 94 seeded from a global metacommunity (Walker and Pace, 2007). However, more recent 3 bioRxiv preprint doi: https://doi.org/10.1101/761262; this version posted September 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 95 work of hypolithic communities have found support for the existence of dispersal 96 limitation between deserts (Archer et al., 2019; Bahl et al., 2011; Caruso et al., 2011). 97 Much of the work investigating lithic habitats over spatial scales has been done using the 98 quartz hypolithic system [19,21,23,25] and only a few global surveys of the endolithic 99 system exist (Friedmann, 1980; Walker and Pace, 2007). While hypolithic communities 100 colonize the underside of quartz rocks at the interface with the underlying soil, endolithic 101 communities colonize a diversity of rock substrates, have been found to be distinct from 102 hypolithic communities within the same local environment (Van Goethem et al., 2016), 103 and can even colonize more extreme environments (Warren-Rhodes et al., 2007a), raising 104 the question of whether the same processes govern the assembly of both lithic habitats. 105 The central question this study seeks to answer is what factors determine the 106 assembly of global desert endolithic communities. A variety of environmental effects 107 have been proposed to influence endolithic community assembly, including macroclimate 108 (Friedmann, 1980), rock geochemistry (Walker and Pace, 2007), and substrate 109 architecture (Meslier et al., 2018), but study limitations and differing methodologies have 110 made it difficult to place the relative importance of these factors. It also remains untested
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