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Living to the High Extreme: Unraveling the Composition, Structure

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Living to the High Extreme: Unraveling the Composition, Structure bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439755; this version posted April 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 1 Living to the high extreme: unraveling the composition, structure, 2 and functional insights of bacterial communities thriving in the 3 arsenic-rich Salar de Huasco – Altiplanic ecosystem. 4 5 6 Castro-Severyn, J1,±; Pardo-Esté, C1,2,±; Mendez, KN3; Fortt, J1; Marquez, S3; Molina, F4; 7 Castro-Nallar, E3; Remonsellez, F1,5 * and Saavedra, CP2 *. 8 9 1 Laboratorio de Microbiología Aplicada y Extremófilos, Facultad de Ingeniería y Ciencias 10 Geológicas, Universidad Católica del Norte, Antofagasta, Chile. 11 2 Laboratorio de Microbiología Molecular, Facultad de Ciencias de la Vida, Universidad 12 Andres Bello, Santiago, Chile. 13 3 Center for Bioinformatics and Integrative Biology, Facultad de Ciencias de la Vida, 14 Universidad Andres Bello, Santiago, Chile. 15 4 Sys2Diag, UMR9005 CNRS ALCEDIAG, Montpellier, France 16 5 Centro de Investigación Tecnológica del Agua en el Desierto-CEITSAZA, Universidad 17 Católica del Norte, Antofagasta, Chile. 18 19 ± Juan Castro-Severyn and Coral Pardo-Esté have contributed equally to this work. Author 20 order was determined both by contribution and in order of increasing seniority. 21 22 *Correspondence: Francisco Remonsellez, [email protected] and Claudia P. Saavedra, 23 [email protected]. 24 25 26 Running title: Altiplanic communities living under arsenic stress. 27 28 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439755; this version posted April 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 29 ABSTRACT 30 Microbial communities inhabiting extreme environments like Salar de Huasco (SH) are 31 adapted to thrive while exposed to several abiotic pressures and the presence of toxic 32 elements like arsenic (As). Hence, we aimed to uncover the role of arsenic in shaping 33 bacterial composition, structure, and functional potential in five different sites in this 34 Altiplanic wetland using a shotgun metagenomic approach. The sites exhibit wide gradients 35 of arsenic (9 to 321 mg/kg), and our results showed highly diverse communities and a clear 36 dominance exerted by the Proteobacteria and Bacteroidetes phyla. Functional potential 37 analyses showed broadly convergent patterns, contrasting with their great taxonomic 38 variability. Arsenic-related metabolism is different among the five communities, as well as 39 other functional categories like those related to the CH4 and S cycles. Particularly, we found 40 that the distribution and abundance of As-related genes increase, following along the As 41 concentration gradient. Approximately 75% of the detected genes for As-metabolism 42 belong to expulsion mechanisms, being arsJ and arsP pumps related to sites with higher As 43 concentrations and present almost exclusively in Proteobacteria. Furthermore, taxonomic 44 diversity and functional potential are reflected in the 12 reconstructed high-quality MAGs 45 (Metagenome Assembled Genomes) belonging to the Bacteroidetes (5), Proteobacteria (5), 46 Cyanobacteria (1) and Gemmatimonadota (1) phyla. We conclude that SH microbial 47 communities are diverse and possess a broad genetic repertoire to thrive under extreme 48 conditions, including increasing concentrations of the highly toxic As. Finally, this 49 environment represents a reservoir of unknown and undescribed microorganisms, with a 50 great metabolic versatility, which needs further study. 51 52 KEY WORDS: Extremophiles, Metagenomics, Arsenic, MAGs, Altiplano. 53 54 55 IMPORTANCE 56 Microbial communities inhabiting extreme environments are fundamental for maintaining 57 the ecosystems; however, little is known about their potential functions and interactions 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439755; this version posted April 16, 2021. 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 4.0 International license. 58 among them. We sampled the microbial communities in Salar de Huasco (SH) in the Chilean 59 Altiplano, a fragile and complex environment that comprises several stresses. We found 60 that microbes in SH are taxonomically diverse; nonetheless, their functional potential seems 61 to have an important convergence degree, suggesting high adaptation levels. Particularly, 62 arsenic metabolism showed differences associated with increasing concentrations of the 63 metalloid throughout the area, and it is effectively exerting a clear and significant pressure 64 over these organisms. Thus, this research´s significance is that we described highly 65 specialized communities thriving in little-explored environments under several pressures, 66 considered analogous of early Earth and other planets, and can have the potential for 67 unraveling technologies to face climate change repercussions in many areas of interest. 68 69 70 INTRODUCTION 71 Extreme environments like high-altitude wetlands select for adaptations in bacterial 72 communities that enable them to thrive. This particular and fragile environment resemble 73 life before the oxygenation of Earth and could serve as models for studying life in other 74 planets. Moreover, microbial communities are critical for maintaining biogeochemical 75 cycles, particularly in extreme environments where there is little presence of other life 76 forms. Therefore, microorganisms are crucial for ecosystems’ health and functioning (1). 77 Salar de Huasco (SH), a high-altitude wetland located in the Chilean Altiplano (20°18’18’’S; 78 68°50’22’’W, Chile) at 3,800 m.a.s.l. is a Ramsar protected site, considered a hotspot for 79 microbial life (2,3). This area is labeled as extreme due to very particular confluence of 80 physicochemical and environmental conditions, like negative water balance, high daily 81 temperature variation, very arid conditions, high salinity, low atmospheric pressure, high 82 solar radiation, presence of arsenic, among other stressors (4, 5, 6, 7, 8, 9). 83 84 In high altitude wetlands, arsenic concentration, moisture availability, and salt 85 concentrations model communities at a small scale (10, 11, 12, 13). The presence of toxic 86 metal(oids), such as arsenic, is one of the main drivers of microbial communities’ 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439755; this version posted April 16, 2021. 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 4.0 International license. 87 composition (14), as an important selection pressure originated from natural geochemical 88 processes or human activities. Also, previous studies have determined that the presence of 89 metal(oids) can influence biogeochemical cycles, namely C, N and S, by promoting specific 90 chemical reactions and the enrichment of chemoautotrophs, for example As(III)-oxidizing 91 bacteria that can couple this process with nitrate reduction (15, 16, 17); thus, making 92 relevant to assess the metabolic potential of indigenous microbes and communities. In the 93 North of Chile, the relationship between volcanism activities and the presence of arsenic is 94 a known feature, this geological process has been attributed to hydrothermal conditions 95 such as geysers and fumaroles in the pre-range and high plateau (5). Besides, bacteria that 96 thrive in these environments exhibit arsenic-related genes, including genes associated with 97 methylation (ArsM), oxidation (AioAB, ArxAB), and dissimilatory reduction (ArrAB) (18). The 98 most common resistance mechanism is based on As(III) extrusion from the cell by efflux 99 pumps, which is commonly coupled with As(V) reduction (19). Thus, making the genes from 100 the ars operon the most abundant arsenic resistance markers; the basic requirements 101 comprises the arsenite efflux (ArsB, Acr3) and arsenate reductase (ArsC) (20). 102 103 Arsenic is a crucial element for the microbial community composition and 104 metagenomic approaches have helped to shed some light on this subject. For instance, in 105 Socompa’s stromatolites arsenic resistance is achieved mainly through reduction and 106 expulsion of As(V) via Acr3 efflux pumps reductases (21, 22). Additionally, others have found 107 that the presence of arsenic influenced the microbial communities, and the Rhodococcus 108 genus was significantly enriched in elevated levels of the metalloid in groundwater (14). 109 Furthermore, arsenic mobilization is distributed across a broad phylogenetic lineage in 110 similar ecosystems, as arrA was detected in Betaproteobacteria, Deltaproteobacteria, and 111 Nitrospirae MAGs (23). Also, although arsenic-related genes are widespread, they are not 112 universal, in particular As metabolism genes such as aioA, arrA, arsM, arxA are less common 113 in the environment compared with acr3, arsB, arsC and arsD (24). 114 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439755; this version
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