Geomicrobial dynamics of Trans-Himalayan sulfur–borax spring system reveals mesophilic bacteria’s resilience to high heat

Roy, Chayan; Mondal, Nibendu; Peketi, A.; Fernandes, Svetlana; Mapder, Tarunendu; Volvoikar, Samida P.; Haldar, Prabir Kumar; Nandi, Nilanjana; Bhattacharya, Tannisha; Mazumdar, Aninda; Chakraborty, Ranadhir; Ghosh, Wriddhiman

doi:10.1007/s12040-020-01423-y

Cited by 5 publications

(55 citation statements)

References 60 publications

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“…The most important genus in this sample was Sulfitobacter. It might be hypothesized that Sulfitobacter appears in such a significant amount in this sample due to the activity that this genus shows to oxidize sulfites (Sorokin, 1995), which are present in high concentrations in the Himalaya region (Roy et al, 2020). Furthermore, this genus has previously been isolated from deep seawater (Song et al, 2019), where the salinity conditions are similar to those in the Himalayan.…”

Section: Discussionmentioning

confidence: 91%

Beyond Archaea: The Table Salt Bacteriome

et al. 2021

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Commercial table salt is a condiment with food preservative properties by decreasing water activity and increasing osmotic pressure. Salt is also a source of halophilic bacteria and archaea. In the present research, the diversity of halotolerant and halophilic microorganisms was studied in six commercial table salts by culture-dependent and culture-independent techniques. Three table salts were obtained from marine origins: Atlantic Ocean, Mediterranean (Ibiza Island), and Odiel marshes (supermarket marine salt). Other salts supplemented with mineral and nutritional ingredients were also used: Himalayan pink, Hawaiian black, and one with dried vegetables known as Viking salt. The results of 16S rRNA gene sequencing reveal that the salts from marine origins display a similar archaeal taxonomy, but with significant variations among genera. Archaeal taxa Halorubrum, Halobacterium, Hallobellus, Natronomonas, Haloplanus, Halonotius, Halomarina, and Haloarcula were prevalent in those three marine salts. Furthermore, the most abundant archaeal genera present in all salts were Natronomonas, Halolamina, Halonotius, Halapricum, Halobacterium, Haloarcula, and uncultured Halobacterales. Sulfitobacter sp. was the most frequent bacteria, represented almost in all salts. Other genera such as Bacillus, Enterococcus, and Flavobacterium were the most frequent taxa in the Viking, Himalayan pink, and black salts, respectively. Interestingly, the genus Salinibacter was detected only in marine-originated salts. A collection of 76 halotolerant and halophilic bacterial and haloarchaeal species was set by culturing on different media with a broad range of salinity and nutrient composition. Comparing the results of 16S rRNA gene metataxonomic and culturomics revealed that culturable bacteria Acinetobacter, Aquibacillus, Bacillus, Brevundimonas, Fictibacillus, Gracilibacillus, Halobacillus, Micrococcus, Oceanobacillus, Salibacterium, Salinibacter, Terribacillus, Thalassobacillus, and also Archaea Haloarcula, Halobacterium, and Halorubrum were identified at least in one sample by both methods. Our results show that salts from marine origins are dominated by Archaea, whereas salts from other sources or salt supplemented with ingredients are dominated by bacteria.

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Section: Discussionmentioning

confidence: 91%

Beyond Archaea: The Table Salt Bacteriome

et al. 2021

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“…Accordingly, our knowledge on microbial adaptation to high temperature is based largely on hot spring isolates that grow in vitro either obligately at ≥80°C (1)(2) or facultatively between 30°C and 80°C (3)(4). Members of mesophilic microbial groups (taxa having no member reported for laboratory growth at >45°C), on the other hand, though unexpected in high-temperature environments, often get stochastically introduced by local geodynamic forces to the hot spring systems (5)(6)(7), where they are detected mostly via sequencing and analysis of metagenomes (6)(7)(8)(9)(10)(11)(12)(13)(14)(15), and sometimes as pure culture isolates (12,16,17). In such a scenario, for a holistic understanding of microbial life's high-temperature adaptation, it becomes imperative to explore the biology of the phylogenetic relatives of mesophilic bacteria which happen to be there in geographically and geologically distinct hot spring habitats.…”

Section: Introductionmentioning

confidence: 99%

“…Potential effects of thermal conditioning on the isolate’s ability to grow or survive at high temperatures were tested by subjecting the organism to different iterations of “heat exposure and withdrawal” cycles. Previous geomicrobiological explorations of Lotus Pond had shown that the snow-melts and denuded soil/sediments, which infiltrate the shallow geothermal reservoir of Puga via local tectonic faults, introduce mesophilic bacteria into the hot spring system (7). Since the soil/sediment systems of the frigid deserts of Ladakh are typically poor in organic carbon (24), and because the vent-water of Lotus Pond has low dissolved solutes concentration (7), the plausible role of oligotrophy in thermal endurance by SMMA_5 was tested via high- temperature incubation in different dilution grades of Reasoner’s 2A (R2A) medium, typically used for growing oligotrophic bacteria (25).…”

Section: Introductionmentioning

confidence: 99%

“…Previous geomicrobiological explorations of Lotus Pond had shown that the snow-melts and denuded soil/sediments, which infiltrate the shallow geothermal reservoir of Puga via local tectonic faults, introduce mesophilic bacteria into the hot spring system (7). Since the soil/sediment systems of the frigid deserts of Ladakh are typically poor in organic carbon (24), and because the vent-water of Lotus Pond has low dissolved solutes concentration (7), the plausible role of oligotrophy in thermal endurance by SMMA_5 was tested via high- temperature incubation in different dilution grades of Reasoner’s 2A (R2A) medium, typically used for growing oligotrophic bacteria (25). Dissolved solutes such as ions of boron and lithium, which are typical of the Puga hot springs including Lotus Pond (7, 14, 23), have been hypothesized previously as the in situ mitigators of the biomacromolecule-disordering effects of heat, and therefore the facilitators of the colonization of high-temperature sites by mesophilic bacteria (14).…”

Section: Introductionmentioning

confidence: 99%

“…Since the soil/sediment systems of the frigid deserts of Ladakh are typically poor in organic carbon (24), and because the vent-water of Lotus Pond has low dissolved solutes concentration (7), the plausible role of oligotrophy in thermal endurance by SMMA_5 was tested via high- temperature incubation in different dilution grades of Reasoner’s 2A (R2A) medium, typically used for growing oligotrophic bacteria (25). Dissolved solutes such as ions of boron and lithium, which are typical of the Puga hot springs including Lotus Pond (7, 14, 23), have been hypothesized previously as the in situ mitigators of the biomacromolecule-disordering effects of heat, and therefore the facilitators of the colonization of high-temperature sites by mesophilic bacteria (14). Accordingly, sodium tetraborate and lithium hydroxide were tested for their potential effects on the high- temperature growth/survival of SMMA_5.…”

Section: Introductionmentioning

confidence: 99%

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Thermal endurance by a hot-spring-dwelling phylogenetic relative of the mesophilic Paracoccus

Mondal

Roy

Chatterjee

et al. 2022

Preprint

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High temperature growth/survival was revealed in a phylogenetic relative (strain SMMA_5) of the mesophilic Paracoccus isolated from the 78-85°C water of a Trans- Himalayan sulfur-borax spring. After 12 h at 50°C, or 45 minutes at 70°C, in mineral salts thiosulfate (MST) medium, SMMA_5 retained ∼2% colony-forming units (CFUs), whereas comparator Paracoccus had 1.5% and 0% CFU left at 50°C and 70°C respectively. After 12 h at 50°C, the thermally-conditioned sibling SMMA_5_TC exhibited ∼1.5 time increase in CFU-count; after 45 minutes at 70°C, SMMA_5_TC had 7% of the initial CFU-count intact. 1000-times diluted Reasoner’s 2A medium, and MST supplemented with lithium, boron or glycine-betaine (solutes typical of the SMMA_5 habitat), supported higher CFU-retention/CFU-growth than MST. With or without lithium/boron/glycine-betaine in MST, a higher percentage of cells always remained viable (cytometry data), compared with what percentage remained capable of forming single colonies (CFU data). SMMA_5, compared with other Paracoccus, contained 335 unique genes, mostly for DNA replication/recombination/repair, transcription, secondary metabolites biosynthesis/transport/catabolism, and inorganic ion transport/metabolism. It’s also exclusively enriched in cell wall/membrane/envelope biogenesis, and amino acid metabolism, genes. SMMA_5 and SMMA_5_TC mutually possessed 43 nucleotide polymorphisms, of which 18 were in protein-coding genes with 13 nonsynonymous and seven radical amino acid replacements. Such biochemical and biophysical mechanisms could be involved in thermal stress mitigation which streamline the cells’ energy and resources towards system-maintenance and macromolecule-stabilization, thereby relinquishing cell-division for cell-viability. Thermal conditioning apparently helped memorize those potential metabolic states which are crucial for cell-system maintenance, while environmental solutes augmented the indigenous stability-conferring mechanisms.IMPORTANCEFor a holistic understanding of microbial life’s high-temperature adaptation it is imperative to explore the biology of the phylogenetic relatives of mesophilic bacteria which get stochastically introduced to geographically and geologically diverse hot spring systems by local geodynamic forces. Here, in vitro endurance of high heat up to the extent of growth under special (habitat-inspired) conditions was discovered in a hot- spring-dwelling phylogenetic relative of the mesophilic Paracoccus species. Thermal conditioning, extreme oligotrophy, metabolic deceleration, presence of certain habitat- specific inorganic/organic solutes, and typical genomic specializations were found to be the major enablers of this conditional (acquired) thermophilicity. Feasibility of such phenomena across the taxonomic spectrum can well be paradigm-changing for the established scopes of microbial adaptation to the physicochemical extremes. Applications of conditional thermophilicity in microbial process biotechnology may be far reaching and multi-faceted.

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