Geomicrobiology: Latest Advances and Prospects

1. Introduction

Geomicrobiology is an interdisciplinary field that involved the study of the role of microbes in the geosphere. This discipline integrates geology, microbiology, ecology, biochemistry, molecular biology, and bioinformatics, in the broadest sense. Some authors have stated that geomicrobiology is a subdiscipline of geobiology, which focuses on the interactions between life and the physical Earth. In contrast, geomicrobiology is more focused on the interactions of microbial life with the environment. Robbins and Konhauser [1], in the Encyclopedia of Geology, fully incorporated geomicrobiology into geobiology, mentioning the term only in the title and once in the first line of the chapter, considering it a subfield. However, many authors prefer to use the term geomicrobiology in a broader sense rather than geobiology.

The earliest geomicrobiological studies date back to the 19th century. Ehrenberg described the biomineralization of iron oxyhydroxydes by Gallionella ferruginea [2], followed by Winogradsky’s research on Beggiatoa and Leptothrix ochracea [3,4]. However, the foundations of geomicrobiology were laid by Lourens G. M. Baas Becking and his book on Geobiology, published in 1934, where he discussed the Earth, organisms, the environment, water, and symbiosis, among other topics [5]. Baas Becking defined geobiology as the study of the relationship between organisms and the Earth and proposed the following principle: “Everything is everywhere, but the environment selects”.

An important contribution to the development of geomicrobiology came from Henry L. Ehrlich, recognized as a pioneer in the field. His research, which began in 1958, extended over several decades and included numerous publications, culminating in his book, published in 1981 and its subsequent editions [6,7].

Since the edition of the three volumes on Environmental Biogeochemistry and Geomicrobiology by Krumbein [8,9,10], and Geomicrobiology by Ehrlich [7], a large number of books and papers have explored various aspects of geomicrobiology over the past half-century. Over the years, geomicrobiology has evolved into a broad field encompassing a wide range of environmental and geochemical significant processes, such as those occurring in deep-sea hydrothermal vents, marine and lacustrine sediments, ore deposits, petroleum reservoirs, deep terrestrial subsurfaces, caves, mines, and extreme acidic environments [11,12,13,14,15,16].

The awareness of a deep microbial biosphere has advanced over the past two decades due to the rapid advances in “omics” techniques and the discovery of an incredible diversity of genotypes and species in habitats above or below the Earth’s surface [17,18]. Other related disciplines such as Geobiotechnology have developed bioremediation solutions over the last decade [19,20].

2. An Overview of Published Articles

This Special Issue compiles five cutting-edge research articles and reviews addressing diverse aspects of geomicrobiology, such as the application of DNA sequencing technologies to caves [21], the search of microbial biosignatures in lava tubes [22], the distribution of the bacterial genus Euzebya in terrestrial environments [23], the potential damage versus protection of lichens in a Cappadocian church [24], and the growth of bacteria in Saharan dust intrusions [25].

Ehrlich, in a memoir about his activities [6], included the subsection “Some broader implications of the foregoing geomicrobiological investigations”. There he refers to the microbial attack of ancient cave art and particularly cited a few papers on the damages to Altamira Cave rock art. Altamira in Spain and Lascaux in France, are perhaps two of the most investigated caves in the world due to the importance of their Paleolithic paintings and the geomicrobiological processes that have led to their deterioration. Some of these processes were originated by new species of bacteria and fungi isolated and described from such caves [26,27,28].

Lascaux Cave was discovered in 1940, and its notoriety lies in the set of 915 figures and numerous geometric symbols from the Solutrean period (17,000 years old). The cave was open to the public in 1948 and aroused great interest among the press and public, with 30,000 visitors per year recorded in 1955, and 100,000 in 1960. The high number of visitors, artificial lighting, and drastic changes in environmental conditions led the cave to suffer several microbial crises caused by the colonization of bacteria and algae and the appearance of green stains that reached a critical level in 1962, leading to its closure. In 2001, another microbial crisis occurred with the appearance of white mycelia caused by the fungus Fusarium solani, and later, black stains on the painted walls due to the colonization by a new fungus, Ochroconis lascauxensis [28]. In 2015, a comprehensive history was published on the problems that occurred at Lascaux after its discovery, and the geomicrobiological research carried out from 2009 till 2015. These studies shed light on the microbial ecology of the cave and the origin of the microbial crises [29]. The other two papers were published in 2016 and 2017 [30,31].

Since 2018 and up to the present, Prof. Y. Moënne-Loccoz’s team has been publishing a series of articles on the geomicrobiology of Lascaux [32,33,34,35,36,37,38,39,40,41]. Bontemps et al. [21] reviewed the application of next-generation DNA sequencing in the study of cave microbiomes, and particularly in Lascaux Cave. The use of metabarcoding and metagenomics provided an exhaustive description of cave microbial diversity in different halls and galleries, or substrata (water, sediments, bedrock, etc.) within a cave, or the effect of cave disturbance in Lascaux and elsewhere. This knowledge is of great importance to understand the global functioning of caves and to provide fundamental information to design cave conservation strategies.

Lava caves or lava tubes are distributed worldwide. These types of caves follow in number and importance to karstic caves and harbor an extremely high biodiversity and variety of secondary mineral and microbial deposits where microbial–mineral interactions can be studied [42,43]. Many lava tubes have been detected on the surface of Mars which suggested that lava caves may be biotopes of potential interest for the search of extraterrestrial life [44,45,46].

Medley et al. [22] studied the microbial communities present in a wide range of speleothems from two geographically distant lava caves from Hawai’i and New Mexico and found large differences in their microbial communities. Actinobacteriota were abundant in New Mexico caves, while Hawaiian caves contained more unclassified bacteria at the genus and species level. Among the Actinobacteriota, the genera Crossiella, Pseudonocardia, Rubrobacter, and Solirubrobacter stand out, and among the unclassified bacteria were recorded wb1-P19, Euzebyaceae, Gemmataceae, Gemmatimonadaceae, and PLTA13.

The four genera of Actinobacteriota found in New Mexico caves were also very abundant in lava caves from California [47]. The abundance of Crossiella is noteworthy, not only in lava caves but also in karstic caves, where it reaches more than 50% of relative abundance in biofilms [48,49]. A recent review also confirmed its abundance in soils and plant rhizospheres and the involvement of Crossiella in biomineralization, and the synthesis of bioactive compounds is of interest for possible biotechnological applications [50].

In most caves, Crossiella is associated with Euzebya and/or uncultured members of the Euzebyaceae family, uncultured Gemmatimonadaceae, wb1-P19, PLTA13, Ga0077536, Nitrospira, and Vicinamibacteraceae [23,49], which were also retrieved by Medley et al. [22] in his caves.

Gonzalez-Pimentel et al. [23] reviewed the abundance and diversity of Euzebyales/Euzebyaceae/Euzebya in terrestrial environments. The origin of this group of bacteria is marine, and no terrestrial Euzebya has been isolated so far. This group of bacteria can thrive under harsh and quasi-extreme terrestrial conditions, including high concentrations of sodium and/or calcium, alkaline pH, highly variable temperatures, and water fluctuations. However, its role in the geochemical cycle of elements is unknown. The data collected indicate that Euzebya is present throughout the biosphere. It is unclear whether these bacteria were dispersed from marine sources to terrestrial environments or if the sequences retrieved from caves and soils correspond to truly terrestrial species that have not yet been described.

In his review, Gonzalez-Pimentel et al. [23] suggested the need to combine high-throughput sequencing with cultivation techniques that replicate environmental conditions to isolate terrestrial Euzebya strains. Finally, the widespread geographical distribution of Euzebya and the interest in understanding its biogeochemical role are expected to drive the optimization of culture media and the isolation of novel species from different terrestrial environments.

The control of biodeterioration and the protection of cultural heritage is a research field of great interest. Microorganisms (including bacteria, fungi, and algae), as well as lichens, mosses, and plants, are major contributors to the deterioration of outdoor monuments. Joseph [51] compiled numerous reports on the involvement of microorganisms in the deterioration and preservation of materials such as stone, metals, graphic documents, textiles, paintings, and glass. In some cases, microorganisms can be used for biological cleaning of surfaces or for consolidation through biomineralization [52,53,54].

Lichens colonize rocks and all types of substrata (including stones, bricks, ceramics, metals, and glass). Lichens are particularly evident when covering the walls of many monuments [55,56,57]. Several authors have discussed the role of lichens in biodeterioration or bioprotection [58,59,60]. This issue presents a multifaceted challenge for conservators. Casanova Municchia et al. [24] delves into this topic through a multidisciplinary approach to investigate the interaction between lichens, microclimatic conditions, and the deterioration of stone in a Cappadocian church. This church is made of tuff with high porosity that deteriorates with freezing–thawing processes. The authors found that tuff surfaces without lichen cover show higher rates of deterioration compared with those colonized by lichens, whose coverage confers a protective effect due to a reduced water penetration. The protective effect was influenced by wall orientation, exposure to wind-driven rain events, and freezing–thawing cycles. The research emphasized the need to integrate conservation strategies for long-term preservation of the cultural heritage including both biological and physical aspects of weathering.

The Sahara Desert is the main source of mineral dust particles transported to the Atlantic Ocean and Europe [61]. Bacteria attached to dust particles can be transported through the atmosphere and dispersed in new environments. These bacteria survive the harsh conditions of long-range airborne transport and are metabolically active [62,63]. Cáliz et al. [64] found a long-lasting influence of airborne North African desert microorganisms in Southern Europe.

Navarro et al. [25] investigated the mineralogical, chemical, and biological composition of Sahara dust particles affecting the Canary Islands. The bacterial composition of dust was dominated by the phyla Pseudomonadota, Bacillota, and Actinomycetota, which were also the dominant phyla in other dust studies [63,65,66,67]. Microscopic observations revealed the presence of iberulites and neoformed kaolinite crystals in association with bacteria and biofilms on mineral particle surfaces. The authors introduced the term “mineral atmospherogenesis” to describe mineral genesis within the atmosphere, and “mineral bioatmospherogenesis” to explain the biotic participation in the neoformation process of kaolinite.

3. Conclusions

This Special Issue on “Geomicrobiology: Latest Advances and Prospects” provides a collection of innovative contributions that focus on current research, new approaches, and recent advances in the field.

Next-generation sequencing (NGS) has greatly enhanced our knowledge of the complex interactions between microbes and the geosphere, shedding light on the metabolic potential and activities of microorganisms in geomicrobiological processes. This includes the identification of biosignatures and secondary mineral formations, which are crucial in the search for extraterrestrial life, a promising research topic of growing interest.

The integration of cutting-edge omics techniques (genomics, proteomics, and metabolomics) in geomicrobiology will enhance our understanding of microbial processes and their implications for geochemical cycles. Such progress opens avenues for exciting discoveries and the development of innovative geobiotechnological solutions.

The study of subsurface microbiomes has highlighted the deterioration processes occurring in rock art caves. Interest in preserving these caves has increased over the last decade due to the harmful impact of leisure tourism and massive visitations. The integrated study of subsurface microbial life, mineralogy, microclimatology, and environmental conditions can provide guidelines for cave conservation.

Despite the harmful effects that microbial activity can provoke on subsurface environments and outdoor monuments, it is worth noting that microorganisms may also provide positive benefits. These include the discovery of novel species and the production and exploitation of new bioactive compounds (antibiotics, surfactants, industrial enzymes, etc.), contributing to the progress of biotechnology. Future geomicrobiology studies should focus on exploring and exploiting the metabolic array of subsurface microorganisms.