Proteomic Signatures of Microbial Adaptation to the Highest Ultraviolet-Irradiation on Earth: Lessons From a Soil Actinobacterium

Abstract

In the Central Andean region in South America, high-altitude ecosystems (3500–6000 masl) are distributed across Argentina, Chile, Bolivia, and Peru, in which poly-extremophilic microbes thrive under extreme environmental conditions. In particular, in the Puna region, total solar irradiation and UV incidence are the highest on Earth, thus, restraining the physiology of individual microorganisms and the composition of microbial communities. UV-resistance of microbial strains thriving in High-Altitude Andean Lakes was demonstrated and their mechanisms were partially characterized by genomic analysis, biochemical and physiological assays. Then, the existence of a network of physiological and molecular mechanisms triggered by ultraviolet light exposure was hypothesized and called “UV-resistome”. It includes some or all of the following subsystems: (i) UV sensing and effective response regulators, (ii) UV-avoidance and shielding strategies, (iii) damage tolerance and oxidative stress response, (iv) energy management and metabolic resetting, and (v) DNA damage repair. Genes involved in the described UV-resistome were recently described in the genome of Nesterenkonia sp. Act20, an actinobacterium which showed survival to high UV-B doses as well as efficient photorepairing capability. The aim of this work was to use a proteomic approach together with photoproduct measurements to help dissecting the molecular events involved in the adaptive response of a model High-Altitude Andean Lakes (HAAL) extremophilic actinobacterium, Nesterenkonia sp. Act20, under artificial UV-B radiation. Our results demonstrate that UV-B exposure induced over-abundance of a well-defined set of proteins while recovery treatments restored the proteomic profiles present before the UV-challenge. The proteins involved in this complex molecular network were categorized within the UV-resistome subsystems: damage tolerance and oxidative stress response, energy management and metabolic resetting, and DNA damage repair.

Community Vertical Composition of the Laguna Negra Hypersaline Microbial Mat, Puna Region (Argentinean Andes)

“…Many HAALs harbor recently reported outstanding microbial mats and microbialites systems, including stromatolites [ 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 ]. Interestingly, studies of these ecosystems have led to the discovery of novel poly-extremophiles, tolerant to high UV radiation and hypersalinity, particularly bacterial and archaeal UV-tolerant strains [ 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 ]. For instance, the UV-tolerant and metal- and metalloids-resistant bacterium Exiguobacterium chiriqhucha str.…”

Environmental metabolomics characterization of modern stromatolites and annotation of ibhayipeptolides

“…We found that metabolites and microorganisms differ between core samples of microbialites submerged in the pool throughout the tidal cycle compared to surface microbialites exposed to flowing water or air between tides. The different chemical profiles observed between submerged and surface exposed core samples could be due to variation in UV exposure [ 73 , 74 ], oxidation, predator grazing, and or age and microbial composition of the microbialite accretions. The new ibhayipeptolide family of cyclic depsipeptides was most abundant in substrate cores of submerged microbialites, and correlated positively with cyanobacterial (OTUs 290, 42) and bacteroidete (OTUs 302, 25) taxa.…”

Environmental metabolomics characterization of modern stromatolites and annotation of ibhayipeptolides

“…The different chemical profiles observed between submerged and surface exposed core samples could be due to variation in UV exposure [73,74], oxidation, predator grazing, and or age and…”