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Metagenome-Assembled Genomes from Monte Cristo Cave (Diamantina, 2 Brazil) Reveal Prokaryotic Lineages As Functional Models for Life on Mars 3 4 Amanda G

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Metagenome-Assembled Genomes from Monte Cristo Cave (Diamantina, 2 Brazil) Reveal Prokaryotic Lineages As Functional Models for Life on Mars 3 4 Amanda G bioRxiv preprint doi: https://doi.org/10.1101/2020.07.02.185041; this version posted July 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 Metagenome-assembled genomes from Monte Cristo Cave (Diamantina, 2 Brazil) reveal prokaryotic lineages as functional models for life on Mars 3 4 Amanda G. Bendia1*, Flavia Callefo2*, Maicon N. Araújo3, Evelyn Sanchez4, Verônica C. 5 Teixeira2, Alessandra Vasconcelos4, Gislaine Battilani4, Vivian H. Pellizari1, Fabio Rodrigues3, 6 Douglas Galante2 7 8 9 1 Oceanographic Institute, Universidade de São Paulo, São Paulo, Brazil 10 2 Brazilian Synchrotron Light Laboratory, Brazilian Center for Research in Energy and Materials, 11 Campinas, Brazil 12 3 Institute of Chemistry, Universidade de São Paulo, São Paulo, Brazil 13 4 Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina, Brazil 14 15 *Corresponding authors: 16 Amanda Bendia 17 [email protected] 18 Flavia Callefo 19 [email protected] 20 21 22 Keywords: Metagenomic-assembled genomes; metabolic potential; survival strategies; quartzite 23 cave; oligotrophic conditions; habitability; astrobiology; Brazil. 24 25 26 Abstract 27 28 Although several studies have explored microbial communities in different terrestrial subsurface 29 ecosystems, little is known about the diversity of their metabolic processes and survival strategies. 30 The advance of bioinformatic tools is allowing the description of novel and not-yet cultivated 31 microbial lineages in different ecosystems, due to the genome reconstruction approach from 32 metagenomic data. The recovery of genomes has the potential of revealing novel lifestyles, 33 metabolic processes and ecological roles of microorganisms, mainly in ecosystems that are largely 34 unknown, and in which cultivation could be not viable. In this study, through shotgun 35 metagenomic data, it was possible to reconstruct several genomes of cultivated and not-yet 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.02.185041; this version posted July 2, 2020. 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. 36 cultivated prokaryotic lineages from a quartzite cave, located in Minas Gerais state, Brazil, which 37 showed to possess a high diversity of genes involved with different biogeochemical cycles, 38 including reductive and oxidative pathways related to carbon, sulfur, nitrogen and iron. Tree 39 genomes were selected, assigned as Truepera sp., Ca. Methylomirabilis sp. and Ca. Koribacter sp. 40 based on their lifestyles (radiation resistance, anaerobic methane oxidation and potential iron 41 oxidation) for pangenomic analysis, which exhibited genes involved with different DNA repair 42 strategies, starvation and stress response. Since these groups have few reference genomes 43 deposited in databases, our study adds important genomic information about these lineages. The 44 combination of techniques applied in this study allowed us to unveil the potential relationships 45 between microbial genomes and their ecological processes with the cave mineralogy, as well as to 46 discuss their implications for the search for extant lifeforms outside our planet, in silica- and iron- 47 rich environments, especially on Mars. 48 49 50 Introduction 51 52 Caves are an example of the terrestrial dark settings that harbor an extensive microbial 53 biomass, biodiversity and geochemical processes, which generates noteworthy morphological and 54 molecular biosignatures, such as the those produced by the recognition of metabolic potentials 55 though specific gene detection (Boston et al., 2001; Hershey and Barton, 2018; Tetu et al., 2013; 56 Wiseschart et al., 2019). Few studies describing the microbial diversity of cave ecosystems have 57 detected the metabolic potential of these microorganisms. In fact, metabolic potential-based 58 recognition of cave microbiome is one of the least scientifically explored strategies (Riquelme et 59 al., 2017). These few studies pointed that, in the absence of light, the microbial community relies 60 on diverse chemolithotrophic metabolisms, as iron oxidation, sulfide oxidation, sulfate reduction, 61 hydrogen oxidation, methanotrophy and methanogenesis (e.g. Osburn et al., 2014; Riquelme et al., 62 2017; Simkus et al., 2016; Wiseschart et al., 2019). Microbial metabolism reported in cave 63 ecosystems from Thailand and Sweden achieved in the Manao-Pee cave and the Tjuv-Ante's cave, 64 respectively, shed light on the value of metabolic potentials for the understanding of microbial 65 diversity, metabolic versatility and adaptation to the extreme conditions of terrestrial subsurface 66 environments (Mendoza et al., 2016; Wiseschart et al., 2019). 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.02.185041; this version posted July 2, 2020. 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. 67 Also, another approach aiming the understanding of microbial dynamics from cave 68 environments is the identification of direct relationship between microorganisms and cave 69 mineralogy, and the corresponding physicochemical signature originated from this interaction. 70 Sauro et al. (2018) suggested that some putative microbial metabolic activities play a role in 71 dissolution and reprecipitation of silica under cave conditions. Additionally, many studies 72 addressed the role played by iron-oxidizing bacteria for the precipitation within Fe-biomineralized 73 filaments and stalks in iron-rich caves, making these bioprecipitate minerals a significant inorganic 74 biosignature (Baskar et al., 2008; Chan et al., 2016; Florea et al., 2011). 75 Two innovative applications of the metabolic potential and diversity in caves ecosystems 76 might be in astrobiology, contributing to elucidate the potential metabolisms in extraterrestrial 77 analogous oligotrophic systems, such as subsurface environments on Mars (Hays et al., 2017; Ortiz 78 et al., 2014). Because of the hostile surface conditions on Mars (e.g. the incidence of intense UV- 79 C radiation) the subsurface environments may offer one of the only accesses to recognizable 80 biosignatures of extant lifeforms (Boston et al., 2001). Also, caves on Earth are particularly 81 interesting analogues because of the better preservation potential of biosignatures over long 82 periods (< 104 years for DNA and <106 years for proteins; Bada et al., 1999), once they may stand 83 under the same physicochemical conditions for long periods (up to millennia time scale; Hershey 84 and Barton, 2018). 85 Another possible application of specific metabolic potentials for astrobiological purposes 86 is related to the characteristics of Mars’ surface. The Martian environment, either superficial or on 87 the subsurface, presents many stressors and challenges for life. The diversity of metabolisms found 88 on caves, especially those that allow the exploration of non-conventional sources of energy and 89 redox potential under extreme conditions, make them promising analogue environments for Mars, 90 and should be further explored. For example, metabolic potentials based on methane and iron may 91 be of great interest, once these elements have been identified on Mars’ surface (e.g. Johnson et al., 92 2016; Rieder et al., 1997; Singer et al., 1979). Recently, sub-annually changes in atmospheric 93 concentration of methane were detected by the Curiosity rover in the area of Gale Crater (Hu et 94 al., 2016) and life was not ruled out among the hypotheses proposed to explain the origin of 95 Martian methane. In addition, these methane-producing regions could harbor a methanotrophic 96 biota. 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.02.185041; this version posted July 2, 2020. 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. 97 Thus, understanding the ecological spectra and adaptation aspects of the metabolic 98 diversity found on caves under oligotrophic settings may be important for i) understanding the 99 several chemolithotrophic metabolisms, including those that better flourish in areas with low 100 carbon offer; ii) expand our knowledge concerning potential areas for habitability; and, again, iii) 101 be useful for life prospection in our neighboring planets and other surfaces. 102 The Brazilian territory harbors several karst ecosystems that are still poorly explored 103 regarding their microbial diversity. The Monte Cristo cave consists of a quartzite cave, presenting 104 aphotic and oligotrophic conditions. It is located in Serra do Espinhaço mountain ridge, near the 105 city of Diamantina, in the State of Minas Gerais, Brazil, an iron-rich area formed by Proterozoic 106 metasedimentary rocks (Vasconcelos, 2014). 107 Based on the exposed before, the main goal of the present research was, through the 108 genome reconstruction of cultivated and not-yet cultivated prokaryotic lineages,
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