Microbial Survival Mechanisms and the
Interplanetary Transfer of Life Through Space
Microbial Survival Mechanisms and the
Interplanetary Transfer of Life Through Space
Journal of Astrobiology and Space Science Reviews, 1, 156-175, 2019

Microbial Survival Mechanisms and the
Interplanetary Transfer of Life Through Space.

Robert J. C. McLean, Ph.D.1, and Malcolm A. C. McLean2,
1Department of Biology, Texas State University-San Marcos, San Marcos, TX, USA.
2University of Colorado at Boulder, Boulder Colorado, USA
(reprinted with permission from the publisher)


Abstract

Panspermia requires that life forms must be able to survive ejection from a planet of origin, transport through space, and introduction to a destination. As microorganisms, primarily Bacteria and Archaea, represent the most numerous, diverse, and stressresistant organisms, they are the most probable candidates for panspermia. the physical stresses related to interplanetary travel include the energy (manifested as heat and shear forces) related to meteorite impact and ejecta; the hard vacuum, temperature extremes, lack of water, and radiation of space; and the heat of atmospheric passage and energy of impact upon arrival. Once in a new location, surviving organisms may be in a situation where they may either encounter a pristine, abiotic environment. Alternatively, they may encounter an environment with other life forms and so may need to compete. Although some issues related to panspermia are speculative, there is an increasing body of experimental literature showing the potential of organisms to survive panspermia-related conditions. While most panspermia investigations are geared towards studying microbial survival, it is possible that transmission of information from one planet to another may occur through transfer of genetic information. In this review, we summarize some biological studies relevant to microbial survival, transport, and growth in the context of panspermia.

Keywords: Bacteria, Archaea, microgravity, stress response, DNA repair, astrobiology, panspermia, spores, planetary protection,

1. Introduction

The biosphere is defined as the region on Earth wherein life can exist. While there are an abundance of plants and animals on the Earth’s surface, the true boundaries of the biosphere are clearly defined by microorganisms such as Bacteria and Archaea. Examples of such environments include hydrothermal vent communities, which are associated with geothermal activity in the deep ocean (Brazelton et al., 2010; Cavanaugh et al., 1992), the upper atmosphere (Miyake et al., 2010; Wainwright et al., 2003, 2010), and deep subsurface environments in terrestrial (Ghiorse and Wilson, 1988) and marine locations (Mason et al., 2009). In the context of physical and chemical constraints, microorganisms are able to withstand extreme environments including ionizing radiation (Gioia et al., 2007), temperatures exceeding 100°C (Brazelton et al., 2010), pH extremes (pH values ranging from <1 – 13) (Konishi et al., 1995; Stevens et al., 1993), limited water (Warren-Rhodes et al., 2006) and nutrients (de la Torre et al., 2003). A number of studies (reviewed in (Costerton et al., 1995) and elsewhere) show how microorganisms are able to enhance their ability to survive in otherwise hostile environments, by growing in surface-adherent, biofilm communities. Thus, one concern about manned or unmanned missions to these or other worlds is the potential to introduce Earth contamination. As a consequence, planetary protection is an important component of mission planning (Osman et al., 2008).

Microbial adaptability and survival is highly relevant to panspermia and the search for extraterrestrial life, i.e. astrobiology (Chyba and Sagan, 1992; Horneck et al., 2010; Hoyle and Wickramasinghe, 1981, 2000; Joseph and Schild, 2010a). In some environments, microbial survival is estimated on the order of centuries and millennia if not longer (Kieft et al., 1998). Microorganisms have been used as models to predict conditions for life on other planets and solar systems (Scalo et al., 2007). While our knowledge of distant planets and solar systems remains limited to distant observations, present technology and resources enables the visitation of nearby regions in the solar system. Of note, Mars (Levin 2010; McKay et al., 1996; Yung et al., 2010), Titan (Naganuma and Sekine, 2010; Sagan et al., 1992), and Europa (Marion et al., 2003; Tyler 2010) have the potential to support current or previous life.

In this review, we will address several key issues related to the ability of microorganisms to be transported from the biosphere of one planet to another (summarized in Table 1). Included in our discussion will be mechanisms for microbial survival following impact and introduction to a new environment. Here, we expand on some issues that are addressed in the paper by Joseph and Schild (2010a).

Table 1. Summary of Microbial Survival Mechanisms of Relevance to Panspermia

2. Microbial Entry Into Space

Human-based space travels aside; there are two likely scenarios for the natural introduction of microorganisms into space. Although there is certainly some possibility of organisms suspended in the atmosphere (Miyake et al., 2010; Wainwright et al., 2003, 2010) being drawn into space (Joseph and Schild 2010a), the more likely mechanism would involve ejecta arising from a collision of a planetary body with a meteorite (Alvarez et al., 1980; Hara et al, 2010; Schulte et al., 2010). While surface material would certainly be present (and likely vaporized) during an impact, there is a high probability of deeper rocks being released as well. On Earth, since microorganisms are present, often in significant numbers (estimates range from 101 - > 108/g material) in both surface and subsurface environments (Balkwill et al., 1988), ejecta from an impact would undoubtedly include microorganisms (Hara et al, 2010).

The energy from an impact can be considerable. An estimate of the energy produced during the Chicxulub asteroid impact (Pope et al., 1997) is on the order of 1031 ergs. This particular asteroid impact is considered to be responsible for the mass extinction at the end of the Cretaceous era (Alvarez et al., 1980; Schulte et al., 2010). As observed in a recent comet impact (Shoemaker-Levy 9) on Jupiter, the ejecta plume from a large impact can extend out several hundred km from the planet surface in spite of a strong gravitational field (Shoemaker et al., 1995). From a microbial perspective, the energy involved in a collision would manifest itself in heat, sudden acceleration, and shear forces.

2.1. Bacterial Structures and Survival

There are a variety of mechanisms by which microorganisms are able to survive extreme physical conditions, likely to be associated with ejection into space. Bacteria and Archaea are small and typically range in size from 0.3 – 2 μm. Also in some environments there can be considerable population density (estimates of surface and subsurface population densities typically range from 101 - >108 / g rock or soil (Balkwill et al., 1988)). The small size and high numbers of microorganisms can result in the possibility of some being shielded and buffered in a protective, insulated microenvironment, during the catastrophic events and energy associated with impact-associated ejection into space. Other issues related to microbial survival during ejection is the shape and structure of the cell wall of bacteria (Beveridge, 1981). The spherical shape of many organisms, such as Staphylococcus sp. and spores produced by Bacillus and Clostridium sp., has been associated with heightened resistance to shearing (Beveridge, 1981). Peptidoglycan, the main structural component of the bacterial cell wall, is very strong with estimates of its strength and elasticity surpassing steel (Beveridge, 1989; Koch and Woeste, 1992). In many microbiology laboratories, bacteria are routinely harvested from liquid suspensions by centrifugation at a relative force sometimes approaching or exceeding 10,000 x gravity (Drew, 1981). Most bacteria, harvested in this fashion remain viable due to the strength of the peptidoglycan cell wall component. In contrast other biological entities, including human blood cells (erythrocytes) that are not protected by peptidoglycan, are broken (lysed) at much lower speeds (above 2000 x gravity).

Some bacteria, notably members of the genera Bacillus and Clostridium can form spores during nutrient limitation. During sporulation, a number of other polymers, including proteins, are also formed and incorporated into the spore wall. Enhanced crosslinking of spore coat polymers has been associated with the enhanced strength and shear resistance of bacterial spores (Driks, 1999), and may also play a role in heat resistance. In the case of bacterial spores, their heightened heat and radiation resistance is related to reduced water content, the presence of specialized proteins, and specialized DNA repair systems (reviewed in Nicholson et al., 2005; Setlow, 2006). Aside from cell wall and spore coat materials, organisms capable of growing and even thriving at elevated temperatures (approaching and even slightly exceeding 100°C) tend to have proteins and other cellular components that are heat resistant, and mechanisms to maintain DNA integrity and repair thermal injury (Brock, 1978).

3. Survival In Space

Once in space, organisms would lose the protection of a planetary atmosphere against solar radiation, and be exposed to vacuum, a lack of gravity and temperature extremes. Liquid water is unable to exist at high vacuum (< 611.73 Pa) and therefore any biological materials, including living cells, would need to survive in the absence of water.

A very common mechanism to store bacteria involves freeze-drying, also called lyophilization (Gherna, 1994). Cells in a freeze-dried state are essentially in a state of suspended animation, and will grow when reintroduced to appropriate growth conditions. Reduced water content is also a factor that can enhance heat and radiation survival in bacterial spores (Setlow, 2006). During the normal processes that occur during spore formation in Bacillus subtilis, much of the heightened resistance of these structures to heat, radiation, and chemicals was attributed to dehydration-induced conformational changes in key proteins and membrane components, rather than quenching of molecular motion (Sunde et al., 2009). These changes are reversible in the presence of adequate water. One would expect that vacuum-induced dehydration would provide even greater protection against physical stresses.

3.1. Heat Survival Mechanisms

Bacteria have a number of mechanisms by which they are able to resist and protect themselves against radiation and heat. When compared to mesophilic bacteria (that typically live between 20-40°C), thermophilic bacteria (optimum growth can exceed 100°C) have greatly enhanced protein and nucleic acid stability (Paz et al., 2004). These mechanisms include an increased cross-linking of proteins and altered DNA structure.

When growing bacteria are subjected to temperatures approaching their upper growth range, cellular damage and death can arise from protein misfolding (denaturation), a loss of membrane integrity and DNA damage. Bacteria, including thermophiles, have a number of stress responses, including producing a variety of heat shock proteins. Early studies showed that bacteria such as Escherichia coli, expressed a number of heat shock genes when they approached their maximum growth temperature; and that bacteria defective in these genes had reduced thermal tolerance (Yamamori and Yura, 1982). Several heat shock genes encode the synthesis of a number of accessory proteins called chaperones.

Chaperones have two main mechanisms of action. Firstly, they prevent misfolding or undesired aggregation of newly synthesized proteins, and secondly correct improper protein folding (Sharma et al., 2009). Of relevance to panspermia, stress response genes have also been identified for cold shock (Jones and Inouye, 1994), starvation-survival (Traxler et al., 2008), oxidative stress and radiation stress (An et al., 2010). In a number of bacteria, many of the stress response genes are involved in more than one stress response, and are considered to be components of a general bacterial stress response (Hengge, 2008).

3.2 Radiation Survival

Radiation survival strategies in bacteria are geared towards prevention of and repair of ionizing radiation-induced damage. The reduced water content in bacterial spores (Sunde et al., 2009) has been associated with the prevention of DNA damage. However, the most radiation resistant organisms known, are non-spore forming bacteria belonging to the genus Deinococcus. These organisms have a number of highly efficient DNA repair mechanisms (White et al., 1999). Bacteria have a number of strategies for fixing nucleic acid damage. Generally these mechanisms involve excision and replacement of faulty DNA bases, and repair of broken strands (Häder and Sinha, 2005). Due to the essential nature of nucleic acids to the survival of bacteria, there are a number of DNA repair mechanisms involved which can function at different growth rates and different proof reading abilities (Bentchikou et al., 2010; Galhardo et al., 2007). Deinococcus radiodurans, the most radiation resistant bacterium known, has an amazing ability to reconstruct its genome from radiation- or desiccation-induced DNA fragments (Bentchikou et al., 2010; Reyes et al., 2010).

There have also been a number of experiments associated with microbial survival under vacuum, radiation, and temperature conditions associated with space. Most of these have occurred in conjunction with spacecraft in Earth orbit, although there is one report of a bacterium, Streptococcus mitis, being isolated from insulation on a camera that had been left on the moon for over 2 years before being recovered during the Apollo 12 lunar mission (Mitchell and Ellis, 1971). Joseph and Schild (2010b) have argued against contamination: "Since a droplet of saliva contains an average of 750 million organisms, if contamination of the lunar TV camera was due to a scientist's inadvertent cough or sneeze, a multitude of related bacteria, and a representation of the entire microbial population would be expected, rather than a single species and a single organism." However, as intriguing as this finding is, contamination during specimen handling cannot be ruled out as an explanation for this organism.

Issues related to radiation survival have involves introducing various microorganisms, to the vacuum and radiation conditions on low Earth orbit (reviewed in Horneck et al., 2010; Taylor, 1974) and so will be addressed briefly here. Of interest, simulated meteorite materials protected microorganisms in one of these studies. Aside from bacterial survival, two higher organisms, the lichens Rhizocarpon geographicum and Xanthoria elegans, originally isolated from alpine and polar environments, also survived (Sancho et al., 2007). In a ground-based experiment, several microorganisms were exposed to simulated radiation, atmospheric and environmental conditions of Mars. A number of spore-forming bacteria were able to survive (Osman et al., 2008), notably Bacillus pumulis, which has been identified as a species of concern with planetary protection, e.g., Earth based microorganisms, potentially contaminating spacecraft (Gioia et al., 2007; Osman et al., 2008).

3.3. Microgravity

One other aspect of the space environment is the absence of gravity. There have been a number of investigations on life forms, including bacteria, during microgravity. These investigations have been conducted in flight as well as in devices that model microgravity (reviewed in Nickerson et al., 2004)). Under these conditions, microorganisms can actually thrive. There was a recent report that the virulence and stress response of one organism, Salmonella enterica, was enhanced during microgravity (Wilson et al., 2007). In a similar investigation with another organism, Pseudomonas aeruginosa, modeled microgravity enhanced the stress responses against reactive oxygen species and heat (Crabbé et al., 2010). In contrast, microgravity reduced the ability of E. coli to repair radiation-induced DNA damage, but DNA repair in the radiation resistant bacterium, D. radiodurans was unaffected (Harada et al., 1998). As is the case in other environments, bacteria such as P. aeruginosa are able to form biofilms under microgravity conditions (McLean et al., 2001), a growth phenomenon well-associated with stress (Costerton et al., 1995). Unlike higher organisms, many microorganisms readily thrive in microgravity environments.

In summary, radiation, temperature extremes, and vacuum conditions of space are considered to be lethal to most microorganisms. However, there is experimental evidence that some organisms under certain conditions are able to survive (Horneck et al., 2010), findings that can support panspermia.

4. Microbial Survival of Impact

Atmospheric passage and impact yield many of the same stresses (heat, gravity, shear forces) as those experienced during entry into space (addressed in section 2). Through a series of planned and accidental events, there are several studies that have directly addressed microbial survival during this phase of panspermia. In one study (Horneck et al., 2001), spores from the bacterium, Bacillus subtilis, were placed between quartz plates and subjected to an explosion-induced, transient shock pressure of 32 GPa. Under these conditions, which mimic those of meteorite impact on Mars, a small number of spores survived (estimated survival rate was 10-4). In a second study (Burchell et al., 2001), Rhodococcus, a genus of non-spore forming bacteria, were attached to a projectile (bullet) that was then fired from a gun onto a target of growth media. Bacterial survival was also noted when spores were placed onto the ablative heat shield of a spacecraft, and exposed to heat during reentry (Brack et al., 2002).

Two investigations were made possible during the tragic destruction of the space shuttle Columbia (NASA mission STS-107) during reentry on February 2003. The estimated speed at loss of signal was 9700 km h-1) (McLean et al., 2006). In one investigation (Szewczyk et al., 2005), viable organisms of the nematode, Caenorhabditis elegans, were recovered from the crash. These organisms had been on the shuttle as part of a biological experiment and were confirmed to be the same organisms that were originally sent on the flight. In a second study, we recovered an actinomycete (non-spore forming bacterium with fungus growth characteristics), Microbispora sp, that is speculated to have flown on this mission as a contaminant (McLean et al., 2006). Figure 1 shows the payload prior to launch (Fig 1A) and following recovery (Fig 1B). Control experiments used in this investigation included a split-sample control, where a portion of the growth media and cultures, sent on the mission were kept in RJCM’s laboratory at room temperature (22°C). During the recovery of the sample at the Kennedy Space Center, a process control was performed to check whether the specimen handling introduced organisms. In spite of these controls, there was no definitive proof of the source of the Microbispora isolate.


Figure 1 – Payload flown on the ill-fated space shuttle Columbia (NASA mission, STS-107) shown before flight (Fig 1A) and outer (Fig 1B) and inner (Fig 1C) containers upon recovery from the crash debris. No penetration damage to the container was observed. A strain of Microbispora, an organism normally associated with soil, was cultured from this debris (McLean et al., 2006).

5. Life After Impact

The majority of biological investigations related to panspermia, have investigated the ability of organisms to survive the environmental and stress conditions during ejection from their origin, transport through space, and impact on their destination. A conservative estimation is that only a small fraction of organisms may survive interplanetary transit and that many of these organisms may be damaged by the stresses they encounter. Microorganisms are a remarkably resilient group, having a number of DNA and other repair mechanisms (Horneck et al., 2010). Should the cells maintain or obtain sufficient resources and encounter a suitable environment, then repair and growth could occur. Growth may occur shortly after introduction to a new environment, or the organisms may remain in a state of dormancy until suitable conditions arise. Depending on the destination, incoming organisms could arrive in a pristine, abiotic environment, which they could colonize. Alternatively, they might arrive in an environment containing other life forms and so face competition. Microbial interactions including competition and cooperation have been studied extensively in many different situations (cf Ramsey and Whiteley, 2009; Rickard et al., 2006).

Another possibility is that the organisms do not survive, but that some portion of their genetic material (DNA or RNA) does. There is a recent line of investigation into the long-term survival and recovery of ancient DNA from sources such as amber (reviewed in Martín-González et al., 2010). A number of microorganisms are able to take up and incorporate DNA from the environment in a process referred to as transformation (Avery et al., 1944; Griffith, 1928). In this context, one cannot discount the possibility of genetic material, surviving transport through space, ultimately becoming incorporated into an organism on a destination planet. Foreign (potentially alien) DNA could introduce new characteristics into a life form on the destination planet (Joseph and Schild 2010a,b). Another possibility is the potential for this new genetic material to alter the control (i.e. regulation) of genes in an organism (Joseph and Wickramasinghe 2010).

Horizontal gene transfer, a process in which segments of new genetic information are transferred from one organism to another, is now recognized as a common occurrence in many bacteria (Joseph 2009; Koonin and Wolf 2008). An example of this is the acquisition of disease-causing (virulence) genes from bacterial viruses (phage) in the intestinal pathogen E. coli O157:H7 (Perna et al., 2001). Genes are transferred not only between bacteria, but between archae and bacteria and viruses, and from viruses and prokaryotes to eukaryotes (Joseph 2009).

6. Concluding Remarks

Panspermia is a very intriguing concept that addresses one of the key scientific questions pertaining to the origin of and uniqueness of life (Hoyle and Wickramasinghe, 1981, 2000; Joseph and Schild, 2010a,b; Lal, 2008). While postulated for some time, there has been a recent upsurge of interest in panspermia through reports of potential extraterrestrial life on meteorites (Gillet et al., 2000; McKay et al., 1996), the presence of organic matter and possible biological markers on comets (Pizzarello, 2004) and other celestial objects (Kwok, 2009). Certainly, as outlined in this article, microorganisms and their component genetic material have the potential to survive interplanetary transport. The number of microorganisms in some environments can be considerable, approaching 108 / g in some materials. As a result, should the extreme physical conditions occurring during panspermia, result in reduction of viability of several orders of magnitude, there would still be the possibility of some organisms surviving. As well, nutrients released from and provided by dead organisms may enhance the survival of others in the microbial community. Dead organisms may also form a protective crust, shielding those within the inner colony from a variety of hazards. Thus there appears to be considerable evidence that microbes could survive an interplanetary journey through space and then colonize the planets upon which they arrive. Nevertheless, it is prudent to be reminded of the quotation by the late Carl Sagan upon the report of possible evidence of life on the ALH84001 meteorite (McKay et al., 1996), "Extraordinary claims require extraordinary evidence".

Acknowledgements: Work in RJCM’s laboratory is supported by a grant from the Norman Hackerman Advanced Research Program. We thank John and Valerie Cassanto and their colleagues of Instrumentation Technology Associates, Exton PA, as well as NASA personnel for making our shuttle experiments possible. As well, we thank Duane Pierson, C Mark Ott, and Cheryl Nickerson for many helpful discussions and advice. We dedicate this paper to the memories of the brave crew of the Space Shuttle Columbia (STS-107), and Carl Sagan, whose work and outreach inspired a generation of future scientists.


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