Abstract
A rigorous exploration of microbial diversity has revealed its presence on Earth, deep oceans, and vast space. The presence of microbial life in diverse environmental conditions, ranging from moderate to extreme temperature, pH, salinity, oxygen, radiations, and altitudes, has provided the necessary impetus to search for them by extending the limits of their habitats. Microbiology started as a distinct science in the mid-nineteenth century and has provided inputs for the betterment of mankind during the last 150 years. As beneficial microbes are assets and pathogens are detrimental, studying both have its own merits. Scientists are nowadays working on illustrating the microbial dynamics in Earth’s subsurface, deep sea, and polar regions. In addition to studying the role of microbes in the environment, the microbe-host interactions in humans, animals and plants are also unearthing newer insights that can help us to improve the health of the host by modulating the microbiota. Microbes have the potential to remediate persistent organic pollutants. Antimicrobial resistance which is a serious concern can also be tackled only after monitoring the spread of resistant microbes using disciplines of genomics and metagenomics The cognizance of microbiology has reached the top of the world. Space Missions are now looking for signs of life on the planets (specifically Mars), the Moon and beyond them. Among the most potent pieces of evidence to support the existence of life is to look for microbial, plant, and animal fossils. There is also an urgent need to deliberate and communicate these findings to layman and policymakers that would help them to take an adequate decision for better health and the environment around us. Here, we present a glimpse of recent advancements by scientists from around the world, exploring and exploiting microbial diversity.
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Introduction
Microbiology has been through many phases of its exploration and exploitation. It got initiated from fermented foods for improving human health and was extensively studied for apprehending disease-causing organisms. Progressively, the scope of microbial activities has been extended to habitats such as the rhizosphere, water bodies, snowy mountains, to marine bodies. However, with the advent of metagenomics, microbes are found to be successfully inhabiting extreme environments like the dead sea, permafrost, hydrothermal vents, hot-spring hyper, alkaline and saline habitat, acid mine drainage, etc. which were considered uninhabitable previously [1]. In addition to being omnipresent in the environment, microbes also inhabit the human skin surface, oral cavity, gastrointestinal tract, and vagina. They are present on animal skins, gut, rumen, etc., and are also found associated with plant tissues. These microbes constitute ecosystems that harbor microbiomes responsible for the hosts' well-being. Many factors ranging from genotype, diet, and environment regulate the microbiota [2]. The dysbiosis of microbiota results in various metabolic disorders [3]. Determining a healthy microbiome for humans, which is still unknown, will have an impact on how diseases will be diagnosed and treated in the future. The inputs from an individualized microbiome can be utilized for devising personalized medications [4]. Nowadays, microbiome studies are being implemented from a global perspective to understand the role of microbes and host interactions.
The recent advancements that have been unearthed related to the microbial diversity and functional dynamics of microbes living in extreme environments of Arctic, Antarctic and Himalayan regions, marine water, and earth subsurface are highlighted in this review. We have also summarized a global perspective of the major advancements in human gut microbiome research. In addition to this, the newer findings related to the role of microbes in bioremediation and plant growth promotion are also documented. Antibiotics have an ecological impact on the microbiota by direct and indirect mechanisms [5]. The composition of the microbiome can be rapidly altered by exposure to antibiotics and the selection of resistant microbes that can be fatal causing acute infections [6]. Thus, studying the antimicrobial resistance and microbiome forms an integral part of the microbial journey. Curiosity-driven microbial diversity research has moved into outer space with improved facilities and financial aid. Now search for microbial life is being expanded to not just other planets of our solar system but also to planets that seem habitable for life in faraway galaxies of the universe. This initiative has provided the necessary impetus to add new dimensions by the Space Agencies such as NASA. NASA has taken up projects to explore Life on Mars. This manuscript provides a glimpse of the diversity of microbial habitats and their roles in achieving a sustainable environment and life (Fig. 1).
Schematic representation of the recent topics covered in this review. The endemic microbes have limitless advantages to humans and the role of microbial literacy in society is enormously important for conveying the knowledge to the masses. Search for microbial signatures is now being conducted on the neighbouring planets (Mars) based on the advances related to microbiology and technology
Microbial Diversity in Polar Regions
The north (Arctic) and south (Antarctic) poles experience maximal cold weather throughout the year and were thought to be uninhabitable by life forms due to extreme climatic conditions. Recent studies have reported that the polar soils harbor distinct patterns of microbial diversity and exhibit dominant phylotypes exclusive to these regions [7]. Due to global warming, the sea ice habitats are shifting and also causing a shift in microbial diversity of these ecosystems, and therefore monitoring the changing dynamics of endemic microbial diversity becomes extremely important [8]. The endemic microbes isolated from the Arctic have been reported to be enriched in hydrocarbon biodegradation potential [9]. In addition to having varied metabolic capabilities, the Arctic soils have been recently reported to harbor antimicrobial resistance genes and virulence factors that differ from previously identified genes [10].
Efforts are also being made to study microbial dynamics and understand the ecology of microbes in Antarctica. The expeditions have been able to isolate culturable bacteria from Antarctic soil since the mid-1990s [11]. Nowadays emphasis is given to the study of the macroclimate of the Antarctic region, which is usually a major deciding factor for species distribution across the globe [12]. Researchers have found that a wide diversity of microbes inhabits the subcontinent of Antarctica, which performs a huge range of ecological functions like biogeochemical cycling and sequestration of anthropogenic CO2 making it available for the global oceanic food web [13]. Currently, major research is being done in the McMurdo Dry Valleys (MDV), one of the utmost extreme environments on earth and the largest ice-free desert region in Antarctica [14]. Despite the harsh conditions, culture-independent methods have revealed a high level of microbial diversity and biomass in the MDV [15]. The diazotrophic cyanobacteria have also been reported in this Antarctic valley, and have been shown to play an instrumental role in nitrogen cycling [16].
In addition to cyanobacteria and actinobacteria [17], a green microalga- Endolithella mcmurdoensis gen. et sp. nov. has also been isolated from McMurdo Dry Valleys (Victoria Land, East Antarctica) during the K020 expedition [18]. So far, E. mcmurdoensis LEGE Z-009 is the only non-axenic isolate found to have cup-shaped chloroplasts, electron-dense bodies, and polyphosphate granules. Furthermore, several species of lichens were isolated from the Ross Sea coast [12]. The biodiversity of cold environments has been shown to harbor important biotechnological enzymes. These microbes are shown to be functionally and phylogenetically distinct from microbes reported from elsewhere in the world. They are reported to use trace gases as an energy source and can also produce metabolic water for hydration needs [19]. Indian expeditions to polar regions have also led to the identification of more than 40 psychrophilic microbes from the Arctic and Antarctic regions that are reported to have biotechnologically important extremozymes [20]. Studying microbial diversity in these areas is immensely crucial to understanding the functioning of these ecosystems and further research will surely identify novel endemic microorganisms having particular characteristics that can be useful for mankind.
Microbial Assets of the Himalayas
Himalayan ranges in India are characterized by the mountains with the highest peaks with constant low temperatures, acidic soil as well as high metal contamination. Himalayan habitat includes wide atmospheric conditions including temperate to high cold climate, nutrition scarcity and harmful UV ray exposure at higher altitudes. Microbial inhabitants of the Himalayan region are generally psychrotolerants and psychrophiles and their biological activities are of utmost importance to maintain the biogeochemical cycling at such extremely low temperatures [21]. Microbes inhabiting such environments have acquired specialized functions and adaptive capabilities and thus, can be potential sources of unique enzymes or bioproducts. For instance, Pseudomonas frederiksbergensis ERDD5:01, an isolate from the glacial stream at Sikkim Himalaya, consists of multiple copies of genes involved in the management of cold stress, oxidative stress, osmotic stress, membrane cell wall alteration and DNA repair mechanism [22]. Being a psychrotrophic bacterium, it grows even at freezing temperatures and can withstand even high UV-C radiation [22]. Another bacterium, Glutamicibacter arilaitensis LJH19, isolated from night-soil compost in northwestern Himalaya, is a psychotropic bacterium that has shown plant growth-promoting (PGP) traits such as siderophore production, Indole acetic acid production, and phosphate solubilization [23]. The enhanced PGP rate has been proven with the increased germination index of pea plants when inoculated with strain LJH19. In addition to this, strain LJH19 could produce amylase, cellulose, and xylanase even at temperatures as low as 10 °C [23].
This evidence suggests the utility of strain LJH19 as a potentially safe bio-inoculant for improved night-soil compost. These bacteria can be further explored for different applications such as Chryseobacterium polytrichastri ERMR1:04 was identified as a producer of cold-adapted lipase. Interestingly, lipase isolated from strain ERMR1:04 was found active at a broad temperature range i.e., 5–65 °C, and proposed the enzyme as a promising biocatalyst [24].
In addition to having psychrotrophic bacteria, the hot springs in the Himalayan region have been also a source of microorganisms belonging to the genus Thermus and Geobacillus having a large number of thermotolerant enzymes with high biotechnological applications [25]. Studies of bacterial diversity at Manikaran and Yumthang thermal springs revealed the rich microbial diversity at the sites including the species of bacterial genera namely Bacillus, Brevibacillus, Burkholderia, Brevundimonas, Geobacillus, Pseudomonas, Rhodanobacter Paenibacillus, Thermoactinomyces, Thiobacillus, and many others [26]. Himalayan hot water spring sites are also the hub of bacteriophages, especially archaeal viruses. Genome level annotations and metagenomic analysis of such sites revealed the active genetic exchange between the viruses and the bacterial population which is considered the probable mode of gene transfer and acquisition of crucial genetic components for better survival of bacterial species [27, 28]. Prevalence of Bdellovibrio spp. at hot springs have been identified which can act and kill the prey bacteria and thus, can be further for develo** live antibiotics [27]. Both thermophilic and psychrotrophic bacteria are potential sources of different thermostable and cold-stable hydrolytic enzymes which indicates the extent of their commercial utility in various medical, agricultural, and industrial applications. The enormous Himalayan microbial diversity is still unexplored due to lack of sampling, difficulties in reaching the sampling sites, and fewer research groups to work in these extreme habitats. However, the growing interest of research groups in Himalayan diversity and increasing knowledge of unculturable genomic methods, and a better understanding of data analysis may fill the gaps in future studies. The microbes and their key biotechnological thermophilic and psychrophilic enzymes are definite assets and contribute to the biobased economy of the world.
Towards Four-Dimensional Microbial Systems Biology in Sea
Dating back to the time when life originated, it was in these water bodies, that harbor hidden treasures. The diversity that lives beneath these least explored sections of the world is the reason behind the smooth functioning of the biogeochemical cycles on which our 1ife depends. Microorganisms inhabit extreme areas under a marine environment, including the continental shelf, intertidal zones, open sea, benthic zone, estuaries, coral reefs, and hydrothermal vents [29]. Adaptation to these extremes requires metabolic diversity and thus they are worth scientific exploration. They are major sources of novel bioactive compounds that may have applications as pharmaceuticals and also biotechnological applications critically promoting the field of marine biology [30, 31]. Marine microorganisms including bacteria, fungi, and archaea have recently become a preferred source to yield novel biomolecules [32]. Microbes including the planktonic archaea are vital for regulating the energy and nutrient cycling along with matter in the marine environments. They are present ubiquitously and show unique symbiotic relationships, unpredictable abundance, biogeochemistry and physiologies [33]. Their response to environmental changes, regulation and interactions are least understood. One of the major reasons for this scenario was the belief in their existence only in extreme habitats [33]. Latest state-of-the-art technologies of genomics, metagenomics, and metabolomics have helped system microbiologists to gain new perspectives on various microbial aspects like their distribution, processes, genes, metabolites and regulation, etc. [34]. The use of Eulerian and Lagrangian survey strategies employing robotic sampling techniques, and coupling it with community-wide microbial gene expression analyses in wild planktonic microbial populations have helped in unraveling some of these mysteries [35]. Findings indicate that various bacterial and archaeal populations in surface waters of oceans show similar, time-variable patterns in gene expressions over a long period. It’s the cross-species coordination of gene expression resulting in coupled metabolism that is induced by specific environmental conditions. An example of such coordination is the summer export to an abyss, the fueling of the ocean’s “biological pump” that delivers nutrients into the deep sea by surface water bacteria. These nutrients are vital for the survival of deep-sea dwellers and the overall ecology of the system [36]. Marine microbial diversity is least explored and is certainly the hope of future biotechnology.
Microbial Dynamics in Earth’s Subsurface
The Earth's subsurface is teeming with new life which can be as ancient as earth but not yet known to us. According to a study, using soil samples from six continents, approximately only 2% of bacterial species account for nearly half of the global soil bacterial communities [37] and less than 1% of the estimated global species of Archaea and bacteria have been taxonomically characterized [38]. Apart from these quantitative restrictions, bacterial culturing favors only a few phylogenetic lineages [39]. While most previous methods relied on culturing techniques, this left behind microbes that could not be cultured in the laboratory, and even those that might behave differently in the laboratory vs. in the wild. As a result, new methodologies must be employed to determine the interactions of these subsurface microbes with the extreme habitats in which they thrive. This, in turn, can aid in better comprehension of the intricate ways in which they influence the biogeochemical cycles. In a recent study, researchers have employed metagenomics to uncover ancient permafrost (20,000–1,000,000 years old) to discern how microbes maintain cellular function in the absence of cell division [40]. Such microbial adaptations included long-term starvation, like membrane stabilization and osmotic stress responses to survive long-time freezing. Another work combined DNA repair techniques with high throughput sequencing (HTS) to obtain 52 Metagenome assembled genomes (MAGs) from sediments spanning a chronosequence of 26–120 kyr. This contributed to a deeper understanding of microbial survival tactics in ancient permafrost. Such research can be applied to other frozen severe settings as well, such as those seen on Mars [41]. Agriculture significantly reduces biodiversity by converting natural habitats to intensely managed systems and by releasing pollutants [42, 43]. There is also a growing gap between the number of species that are identified by the metagenomics technique and hence proposals for establishing nomenclature rules for unculturable taxa primarily based on sequence information are proposed [38, 44].
The high throughput omics-based techniques like metagenomics, transcriptomics, meta-metabolomics, and meta-proteomics help in generating metagenome-assembled genomics that is being used to improve culturomics techniques to culture the difficult to culture bacteria [44]. However, the cost of conducting omics studies is still expensive. Attempts are being made to link the known genes of important microbes to their functions in-situ by using functional genomics coupled with microarray techniques [45]. Zhou and coworkers have developed a GeoChip covering more than 10,000 genes spanning 150 functional groups involved in nutrient cycling, organic contaminant degradation, metal resistance, etc. to study the microbial community present in a particular niche by combining high-throughput methods and experiments [46]. Additionally, this technology is being implemented to offer basic research solutions for global issues such as carbon sequestration, environmental remediation, bioenergy solutions, etc. Geochip can also be used for decoding the dynamics of microbial communities and the basic mechanisms behind these fluctuations [47]. This has led to the development of newer methods and techniques for studying evolutionary genomics in conjunction with long-term laboratory experiments coupled with omics-based approaches [107]. Another important unanswered question is the determination of a healthy microbiome for humans and various domesticated animals [64]. Microbes are an integral part of our lives and the future holds several treasures of information that will help us to lead a better and healthy life. The future surely holds new insights linked to the identification of microbes both beneficial and dangerous for mankind, there will be improvements in diagnostic procedures and revamped treatment procedures. This knowledge will help us in solving various problems related to bioremediation, enhancing crop yield to feed the increasing human population and development of personalized medicines. In brief, microbiological journey is progressing in the right direction and the insights gained are providing critical intelligence for the betterment of mankind.
Conclusions
Microbiology as a science is also gaining realization as the major field of study. We have come up a long way in deciphering the presence and potential of microbes. Now this journey of microbiological sciences is expanding to all the parts of the earth and also to other planets of our solar system. The extreme biomes that are earlier thought to be uninhabitable, are now deciphered as a unique reservoir with great biotechnological potential. Still, there are questions related to microbial life that are to be answered. To unravel unfolded mysteries further, microbiology needs rapid microbial detection techniques. The growing metagenomic knowledge with advanced sequencing and analytical tools will lead to the characterization of many novel communities of micro-organisms from these untapped environments gifting humankind beneficial products. The search for life on other planets is just beginning to provide answers about our evolution. Further research on extraterrestrial existence with microbiological tools would carve a new turn in our understanding. More recent advancements are being made about the role of microbes in bioremediation and plant growth promotion. With global threats of pandemics, AMR, bioterrorism, and food security, there is an urgent need for microbial literacy worldwide in rural and urban sectors that will result in making correct decisions by mankind and policymakers worldwide. The biotechnological aspects and the impact of the ubiquitous microbes on human health surely will help improve the biobased economy of the country by making India self-reliant and also reducing the load of expenditure done on controlling the spread of infectious diseases and AMR.
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Sood, U., Dhingra, G.G., Anand, S. et al. Microbial Journey: Mount Everest to Mars. Indian J Microbiol 62, 323–337 (2022). https://doi.org/10.1007/s12088-022-01029-6
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DOI: https://doi.org/10.1007/s12088-022-01029-6