Earth’s Aerial Biosphere Offers Insights into Venusian Microbial Survival

Authors: (1) Sara Seager, Departments of Earth, Atmospheric and Planetary Sciences, Physics, Aeronautics and Astronautics, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA; (2) Janusz J. Petkowski, Department of Earth; (3) Peter Gao, Department of Astronomy, University of California at Berkeley, California, USA; (4) William Bains, Department of Earth; (5) Noelle C. Bryan, Department of Earth; (6) Sukrit Ranjan, Department of Earth; (7) Jane Greaves, School of Physics and Astronomy, Cardiff University, Cardiff, United Kingdom and Institute of Astronomy, Cambridge University, Cambridge, United Kingdom. Table of Links Abstract and 1. Introduction and Overview Challenges and Assumptions for Life in the Venusian Clouds A Proposed Cycle for Venusian Aerial Microbial Life Discussion Summary, Acknowledgments, Author Disclosure Statement, Funding Information, and References 4. Discussion With our hypothesized life cycle articulated, we now turn to a discussion for further context. 4.1. Earth’s aerial biosphere Clouds on Earth harbor a diverse species of microbial life, including bacteria, archaea, eukaryotes, and viruses (Amato et al., 2017, 2019). On Earth, most microbes reside inside cloud liquid water droplets but some are free-floating in the atmosphere. In the past, scientists were skeptical of microbial survival in Earth’s clouds, because of: UV-fluxes, low temperatures, severe desiccation, and the transient and fragmented status of cloud cover that could lead to a sudden loss of habitat. Within the past decade, however, this harsh view of Earth clouds as a habitat for life has improved. Modern molecular biological techniques such as metagenomics and metatranscriptomics have given new insights into microbial diversity and metabolic functioning, especially for microbes residing inside cloud water droplets (Amato et al., 2017, 2019) (Fig. 4). The transport of microbes from Earth’s surface up into the clouds is now known to be a common phenomenon (Vaı¨tilingom et al., 2012; Amato et al., 2017; Bryan et al., 2019) (Fig. 5). Earth’s cloud ‘‘aerial biosphere’’ is believed to serve as a temporary refuge during long distance transportation across the planet, rather than a permanent habitat for microbial life. Microbes are eventually deposited to the surface by precipitation (Vaı¨tilingom et al., 2012). On Earth, bacterial aerosols in the troposphere remain aloft on average for 3 to 7 days (Burrows et al., 2009), which is enough time for microbes to be transported over long distances, across whole continents and oceans (Barbera´n et al., 2015; Griffin et al., 2017; Sˇantl-Temkiv et al., 2018). Earth bacteria swept up from the surface have been postulated to act as CCN of water clouds (Sattler et al., 2001; Bauer et al., 2003) or trigger ice nucleation. However, this has not been proven to occur outside the lab; calcium carbonate shells (coccoliths) are as yet the only known biological source that can act as CCN (Trainic et al., 2018). Earth’s clouds are a challenging ecological niche for permanent habitation because of their transient and fragmented nature (in contrast to Venus’ permanent and continuous cloud cover). In addition to the fact that Earth’s surface is habitable, there is no evolutionary pressure exerted on the microbial biosphere on Earth to adopt a life cycle permanently sustained in the clouds. Rather, the evolutionary selection has likely been focused on temporary survival in the clouds (including cloud-specific complex metabolic functions) in anticipation for the eventual deposition on the habitable surface of the planet. For clouds to be a permanent habitat, active cell division would have to occur in the clouds. Metatranscriptomics studies on Earth’s aerial biosphere have not identified transcripts related to active DNA replication and cell division, suggesting that DNA replication and cell division are not performed in situ by metabolically active cells in the cloud biosphere. Therefore, Earth’s microorganisms are using the clouds to migrate to new habitats, not to stay in the clouds and reproduce. This implies that the cloud droplets are only transiently inhabited by microbial life and that the aerial biosphere is intimately tied to the habitable surface. Although there is no direct evidence of active cell division available in situ in cloud droplets, there is ample evidence for a surprisingly physiologically active and diverse metabolism of microbes in cloud droplets (Amato et al., 2019). Diverse physiological and biochemical strategies of microbes have been identified that seem to be direct, specific adaptations to cloud droplet environment. Those include protection against oxidants, osmotic pressure variations, the synthesis of cryoprotectants to fight extreme cold, or production of metal ion scavengers and biosurfactants (Amato et al., 2017, 2019) (Fig. 4). Earth cloud droplets could, therefore, greatly extend the layer of the biosphere that is at least transiently inhabited by metabolically active life on Earth. Further, clouds are definitively not the upper limit of the biosphere, as there is evidence for free-floating viable microbial isolates in the stratosphere up to 38 km (Bryan et al., 2019). We emphasize, however, that, contrary to cells inhabiting cloud droplets, such free-floating microbial life will only survive a few days due to severe desiccation and high UV exposure (Bryan et al., 2019) (see Section 2.1 for discussion of the specific challenges for free-floating microbial life in the atmosphere). The characteristics that enable certain microorganisms to retain viability in clouds are likely attributed to the selective advantage of being able to survive long-distance transport to new surface habitats that is provided by temporary cloud droplet colonization (Fig. 5). The habitability of the Earth surface likely squashed any potentially significant evolutionary advantages that might be gained from permanent cloud colonization. In contrast to Earth, the lack of habitable surface on Venus would force hypothetical microbes to live in the clouds permanently. Therefore, the natural selection pressure on Venus would be directed toward evolutionary strategies that allow life to colonize clouds permanently and not just transiently as it is on Earth. This forms the basis for our life cycle hypothesis: that the entire life cycle of Venusian life, including genetic material replication and cell division, must occur in the only temperate region of Venus—the clouds. 4.2. Active mechanisms for remaining aloft? Throughout the article, we have assumed that the passive mechanisms of air movement drive our proposed life cycle, enabling microbes to remain aloft in the Venusian temperate zone for part of their life cycle. Active mechanisms might evolve but are beyond the scope of this article. Active mechanisms could perpetuate life in the clouds of Venus in four ways. First, life could be part of the life cycle proposed here, actively propelling the desiccated spores upward over many kilometers. Second, life could maintain falling droplets in the cloud layer (i.e., propel falling droplets upward). Third, life could expel living cells or spores from falling droplets in the cloud layer, which the vertical air movements discussed earlier could then mix throughout the clouds to colonize other, smaller droplets. On Earth some microscopic fungi and bacteria are capable of pushing fruiting bodies through the surface tension of water droplets and into the air phase before releasing spores through the air to new habitats, in the process successfully breaking surface tension at the water–air interface (Talbot, 1999; Elliot and Talbot, 2004). This is a relatively complex, active mechanism, and it only works over cm to m distance scales. Lastly, fourth, at least in principle, life could be droplet-independent macroscopic life with the ability to self-transport. 4.3. On biomass and fluxes in the Venusian lower haze layer For our proposed life cycle to be viable, microbes within droplets must reproduce in large enough numbers (e.g., each droplet falling down could have dozens of organisms in it) to balance the spores lost from the haze layer. We imagine the Venus atmosphere as three boxes: the clouds, the lower haze, and the deep hot atmosphere that acts as a sink to the microbes. In the clouds, the total mass of microbes can increase by uptake of nutrients from the droplet or ambient atmosphere, leading to cell division, such that the downward flux of cells from the clouds can be larger than the upward flux from the lower haze. The excess downward flux of cells, however, must balance the downward flux from the lower haze into the deep atmosphere, where the microbes are lost forever to fatally high temperatures. If we conservatively imagine that 10 times more spores are lost to the lower atmosphere than get transported back up (and further accounting for some spores that just die off), each cell would have to divide, say four times (reaching 16 cells per large droplet). This is very reasonable, considering that in Earth’s anaerobic conditions, cell division can be as short as the order of hours, not the months or years that the droplets remain in the cloud layer. The Venusian atmosphere dynamics, especially in the lower haze layer, are not well enough understood to have any certainty to work out mass or flux balance. All we can say is that upward mixing by gravity waves is a way to move small particulate biomass upward, and would have to approximately equal the planet-wide but slow sedimentation of biomass trapped inside droplets. Vertical transport and fluxes, including Hadley cell transport at the equator and poles, definitely require further study. This paper is available on arxiv under CC BY 4.0 DEED license. Authors: (1) Sara Seager, Departments of Earth, Atmospheric and Planetary Sciences, Physics, Aeronautics and Astronautics, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA; (2) Janusz J. Petkowski, Department of Earth; (3) Peter Gao, Department of Astronomy, University of California at Berkeley, California, USA; (4) William Bains, Department of Earth; (5) Noelle C. Bryan, Department of Earth; (6) Sukrit Ranjan, Department of Earth; (7) Jane Greaves, School of Physics and Astronomy, Cardiff University, Cardiff, United Kingdom and Institute of Astronomy, Cambridge University, Cambridge, United Kingdom. Authors: Authors: (1) Sara Seager, Departments of Earth, Atmospheric and Planetary Sciences, Physics, Aeronautics and Astronautics, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA; (2) Janusz J. Petkowski, Department of Earth; (3) Peter Gao, Department of Astronomy, University of California at Berkeley, California, USA; (4) William Bains, Department of Earth; (5) Noelle C. Bryan, Department of Earth; (6) Sukrit Ranjan, Department of Earth; (7) Jane Greaves, School of Physics and Astronomy, Cardiff University, Cardiff, United Kingdom and Institute of Astronomy, Cambridge University, Cambridge, United Kingdom. Table of Links Abstract and 1. Introduction and Overview Abstract and 1. Introduction and Overview Challenges and Assumptions for Life in the Venusian Clouds A Proposed Cycle for Venusian Aerial Microbial Life Discussion Summary, Acknowledgments, Author Disclosure Statement, Funding Information, and References Challenges and Assumptions for Life in the Venusian Clouds Challenges and Assumptions for Life in the Venusian Clouds A Proposed Cycle for Venusian Aerial Microbial Life A Proposed Cycle for Venusian Aerial Microbial Life Discussion Discussion Summary, Acknowledgments, Author Disclosure Statement, Funding Information, and References Summary, Acknowledgments, Author Disclosure Statement, Funding Information, and References 4. Discussion With our hypothesized life cycle articulated, we now turn to a discussion for further context. 4.1. Earth’s aerial biosphere 4.1. Earth’s aerial biosphere Clouds on Earth harbor a diverse species of microbial life, including bacteria, archaea, eukaryotes, and viruses (Amato et al., 2017, 2019). On Earth, most microbes reside inside cloud liquid water droplets but some are free-floating in the atmosphere. In the past, scientists were skeptical of microbial survival in Earth’s clouds, because of: UV-fluxes, low temperatures, severe desiccation, and the transient and fragmented status of cloud cover that could lead to a sudden loss of habitat. Within the past decade, however, this harsh view of Earth clouds as a habitat for life has improved. Modern molecular biological techniques such as metagenomics and metatranscriptomics have given new insights into microbial diversity and metabolic functioning, especially for microbes residing inside cloud water droplets (Amato et al., 2017, 2019) (Fig. 4). The transport of microbes from Earth’s surface up into the clouds is now known to be a common phenomenon (Vaı¨tilingom et al., 2012; Amato et al., 2017; Bryan et al., 2019) (Fig. 5). Earth’s cloud ‘‘aerial biosphere’’ is believed to serve as a temporary refuge during long distance transportation across the planet, rather than a permanent habitat for microbial life. Microbes are eventually deposited to the surface by precipitation (Vaı¨tilingom et al., 2012). On Earth, bacterial aerosols in the troposphere remain aloft on average for 3 to 7 days (Burrows et al., 2009), which is enough time for microbes to be transported over long distances, across whole continents and oceans (Barbera´n et al., 2015; Griffin et al., 2017; Sˇantl-Temkiv et al., 2018). Earth bacteria swept up from the surface have been postulated to act as CCN of water clouds (Sattler et al., 2001; Bauer et al., 2003) or trigger ice nucleation. However, this has not been proven to occur outside the lab; calcium carbonate shells (coccoliths) are as yet the only known biological source that can act as CCN (Trainic et al., 2018). Earth’s clouds are a challenging ecological niche for permanent habitation because of their transient and fragmented nature (in contrast to Venus’ permanent and continuous cloud cover). In addition to the fact that Earth’s surface is habitable, there is no evolutionary pressure exerted on the microbial biosphere on Earth to adopt a life cycle permanently sustained in the clouds. Rather, the evolutionary selection has likely been focused on temporary survival in the clouds (including cloud-specific complex metabolic functions) in anticipation for the eventual deposition on the habitable surface of the planet. For clouds to be a permanent habitat, active cell division would have to occur in the clouds. Metatranscriptomics studies on Earth’s aerial biosphere have not identified transcripts related to active DNA replication and cell division, suggesting that DNA replication and cell division are not performed in situ by metabolically active cells in the cloud biosphere. Therefore, Earth’s microorganisms are using the clouds to migrate to new habitats, not to stay in the clouds and reproduce. This implies that the cloud droplets are only transiently inhabited by microbial life and that the aerial biosphere is intimately tied to the habitable surface. Although there is no direct evidence of active cell division available in situ in cloud droplets, there is ample evidence for a surprisingly physiologically active and diverse metabolism of microbes in cloud droplets (Amato et al., 2019). Diverse physiological and biochemical strategies of microbes have been identified that seem to be direct, specific adaptations to cloud droplet environment. Those include protection against oxidants, osmotic pressure variations, the synthesis of cryoprotectants to fight extreme cold, or production of metal ion scavengers and biosurfactants (Amato et al., 2017, 2019) (Fig. 4). Earth cloud droplets could, therefore, greatly extend the layer of the biosphere that is at least transiently inhabited by metabolically active life on Earth. Further, clouds are definitively not the upper limit of the biosphere, as there is evidence for free-floating viable microbial isolates in the stratosphere up to 38 km (Bryan et al., 2019). We emphasize, however, that, contrary to cells inhabiting cloud droplets, such free-floating microbial life will only survive a few days due to severe desiccation and high UV exposure (Bryan et al., 2019) (see Section 2.1 for discussion of the specific challenges for free-floating microbial life in the atmosphere). The characteristics that enable certain microorganisms to retain viability in clouds are likely attributed to the selective advantage of being able to survive long-distance transport to new surface habitats that is provided by temporary cloud droplet colonization (Fig. 5). The habitability of the Earth surface likely squashed any potentially significant evolutionary advantages that might be gained from permanent cloud colonization. In contrast to Earth, the lack of habitable surface on Venus would force hypothetical microbes to live in the clouds permanently. Therefore, the natural selection pressure on Venus would be directed toward evolutionary strategies that allow life to colonize clouds permanently and not just transiently as it is on Earth. This forms the basis for our life cycle hypothesis: that the entire life cycle of Venusian life, including genetic material replication and cell division, must occur in the only temperate region of Venus—the clouds. 4.2. Active mechanisms for remaining aloft? 4.2. Active mechanisms for remaining aloft? Throughout the article, we have assumed that the passive mechanisms of air movement drive our proposed life cycle, enabling microbes to remain aloft in the Venusian temperate zone for part of their life cycle. Active mechanisms might evolve but are beyond the scope of this article. Active mechanisms could perpetuate life in the clouds of Venus in four ways. First, life could be part of the life cycle proposed here, actively propelling the desiccated spores upward over many kilometers. Second, life could maintain falling droplets in the cloud layer (i.e., propel falling droplets upward). Third, life could expel living cells or spores from falling droplets in the cloud layer, which the vertical air movements discussed earlier could then mix throughout the clouds to colonize other, smaller droplets. On Earth some microscopic fungi and bacteria are capable of pushing fruiting bodies through the surface tension of water droplets and into the air phase before releasing spores through the air to new habitats, in the process successfully breaking surface tension at the water–air interface (Talbot, 1999; Elliot and Talbot, 2004). This is a relatively complex, active mechanism, and it only works over cm to m distance scales. Lastly, fourth, at least in principle, life could be droplet-independent macroscopic life with the ability to self-transport. 4.3. On biomass and fluxes in the Venusian lower haze layer 4.3. On biomass and fluxes in the Venusian lower haze layer For our proposed life cycle to be viable, microbes within droplets must reproduce in large enough numbers (e.g., each droplet falling down could have dozens of organisms in it) to balance the spores lost from the haze layer. We imagine the Venus atmosphere as three boxes: the clouds, the lower haze, and the deep hot atmosphere that acts as a sink to the microbes. In the clouds, the total mass of microbes can increase by uptake of nutrients from the droplet or ambient atmosphere, leading to cell division, such that the downward flux of cells from the clouds can be larger than the upward flux from the lower haze. The excess downward flux of cells, however, must balance the downward flux from the lower haze into the deep atmosphere, where the microbes are lost forever to fatally high temperatures. If we conservatively imagine that 10 times more spores are lost to the lower atmosphere than get transported back up (and further accounting for some spores that just die off), each cell would have to divide, say four times (reaching 16 cells per large droplet). This is very reasonable, considering that in Earth’s anaerobic conditions, cell division can be as short as the order of hours, not the months or years that the droplets remain in the cloud layer. The Venusian atmosphere dynamics, especially in the lower haze layer, are not well enough understood to have any certainty to work out mass or flux balance. All we can say is that upward mixing by gravity waves is a way to move small particulate biomass upward, and would have to approximately equal the planet-wide but slow sedimentation of biomass trapped inside droplets. Vertical transport and fluxes, including Hadley cell transport at the equator and poles, definitely require further study. This paper is available on arxiv under CC BY 4.0 DEED license. This paper is available on arxiv under CC BY 4.0 DEED license. available on arxiv

Earth’s Aerial Biosphere Offers Insights into Venusian Microbial Survival

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