Mobility Encoded in the Genome
A FROZEN LABORATORY TO STUDY GENETIC MOBILITY
I am at 11,000 meters above ground, on the move again, traveling between where I am from to where I live, and never quite sure which is home. Below me, the Atlantic. We must be close to Greenland now. Even from this height, I can see whitecaps moving across the ocean surface and, occasionally now, pieces of sea ice floating southward. I have been fascinated by sea ice for as long as I can remember. Parts of that fascination might be grounded in the apparent discrepancy between something appearing both solid and hard, but also fragile and delicate. Nature documentaries of the poles looked like insights into alien worlds to me. Seeing it now gives me mixed feelings as I know that these beautiful, glistening frozen bodies are inevitably drifting towards the end of their life.
Sea ice is a transient feature that forms from seawater and can travel great distances as it is being pushed across the surface ocean by winds and currents. Over its lifetime, it experiences drastic environmental changes: months of dark polar night when the sun never rises and bright summer months when the sun never sets, extremely low temperatures in the winter and melting periods in the summer. A look inside the ice can often provide clues on where it traveled and what it encountered along the way. Sediment inclusions suggest ice formation close to a coast, a fresh layer can point to a previous warming event and a deformation indicates where two pieces of ice collided. It is as if sea ice carries a memory of its journey.
Unlike freshwater ice cubes that we keep in our freezers and add to drinks, sea ice forms from salty water which affects its freezing dynamics and results in ice of higher porosity. The reason for that is that salt is being expelled during ice crystallization and is then entrapped and concentrated inside narrow channels and pockets within the growing ice matrix. High salt concentrations depress the freezing point of water allowing for the retention of liquid water at subzero temperatures. These salty liquids are called brines.
Inside the brines, millions of microbes, invisible to the naked eye, live their secret lives under seemingly harsh and inhospitable conditions. Like the salt, microbes, as well as viruses, get concentrated during the freezing process and then find themselves in a spatially constrained setting among other organisms and particles whose paths would cross less frequently in the open ocean (Boetius et al., 2015). This, to me, is where the magic happens: A natural laboratory to study microbial interactions and genetic exchange.
TRADING UNITS OF GENETIC INFORMATION
But wait, let’s take a step back. Why are we talking about microbes and viruses now? It seems like most of us heard enough news and conversations on the topic over the last three years. The COVID-19 pandemic has been affecting us and the world as we knew it to an extent that few of us were able to foresee. For many it brought sickness, death, personal and material losses, it abridged our freedom to move, travel and socialize, and was often accompanied by a lingering fear of not knowing how the situation would evolve. Thus, many have come to associate viral outbreaks with catastrophe, unaware that viruses play an integral role in our evolution and survival.
Viruses are everywhere and inherent to all forms of life. They are the most abundant biological entities on Earth and are even hundreds of millions of times more numerous than the stars in the universe. For some it might be shocking to learn that there are more viruses in just one liter of surface seawater (~10^10) than there are people on this planet (7.9 × 10^9) (Breitbart, 2012).
Most of these are not harmful to humans, which explains why swallowing about a billion viruses whenever we swim in a lake or an ocean is typically not an issue. Strictly speaking, viruses are not even alive. They are mobile pieces of genetic material packed in a protein coat, and are fully dependent on a suitable host who provides building blocks to reproduce. Hosts can range from the smallest microbe to the largest mammal but are fairly specific for any given virus. In the oceans, it has been estimated that viruses succeed in infecting bacteria a mind-boggling 10^24 times per second. Most of these infections are lethal, resulting in the lysis of the cell and the release of new viruses to the environment, but some are also neutral or even beneficial. For every infection, there is a small chance of genetic exchange between the virus and its host, meaning that the virus could take up genes from one host genome and carry them to a subsequent host, or leave behind some of its own genetic material enriching the genetic makeup of the host. In a way, viruses are the epitome of mobility: protein-shelled vectors of genetic information whose sole purpose is to travel from one host to the next and reproduce.
Our own genome is an excellent attestant to the long-lasting and complicated evolutionary relationship that exists between viruses and their hosts: While we can clearly suffer from viral infection, the human genome also contains at least 100,000 pieces of ancient viral genetic material that together account for about 8% of our genome. Some of the genes of this viral gene pool are responsible for the evolution of our placenta (Marshall, 2023), others encode a protein that is thought to play a vital role in the brain’s ability to store new information, and some may boost our immune system, potentially protecting us from modern viruses. The multifaceted roles that these «fossil viruses» play for our health are, however, far from being fully understood, which is at once exciting but also hard to comprehend.
When working on environmental samples (as opposed to working on human health or animal health), there are even more unknowns. For many areas of our oceans, we are still in an exploration phase: every new study will discover hundreds or thousands of novel viruses, or to put it simply, reveal unrecorded mobile genetic information. We can check whether these viruses are known or unknown by comparing their genetic information against existing databases. This might be reminiscent of the supermarket checkout process when items on the conveyor belt produce this comforting little beep sound when they get recognized by the scanner. Yet, in the case of our environmental viruses, hardly any of them have a barcode, thus need to be tediously added by hand. Databases that collect genetic information of environmental microbes and viruses have been growing exponentially, as has our appreciation of the environmental impacts of marine viruses for evolution and biogeochemistry.
After it was recognized that they can not only kill as much as 40% of bacterial cells in the oceans in a day (Suttle, 2005), but also mobilize genetic information and manipulate major ecosystem processes, they were coined «the puppet masters» (Breitbart et al., 2018) of marine microbes. A prime example of this puppet-mastery was the discovery of genes relevant for photosynthesis encoded in viral genomes.
One of them is a type of bacteria called Prochlorococcus, which alone is thought to be responsible for 20% of the oxygen in the atmosphere, thus essential to our survival. At some point in their evolutionary history, viruses of Prochlorococcus have mobilized genes from their host that are critical for photosynthesis (Lindell et al., 2004). During infection they can now boost the photosynthesis rate and fitness of their host, ultimately benefiting their own reproduction (Zimmerman et al., 2019). This also means that parts of the oxygen we breathe is a by-product of an ancient gene transfer event and ongoing viral infection in the oceans.
Ice Core Close Up
MOBILITY AT THE MICROSCALE
If we assume an even distribution and an abundance of bacterial cells in the order of 10^6 bacteria and 10^7 viruses per milliliter in the surface ocean, then the distance between a bacterium and its next bacterial neighbor would be 100 μm and approximately 26 μm to the nearest virus (Stocker, 2015). What sounds like a laughably small distance to us, would correspond to about 250 m and 65 m when scaled to the average human body size. However, one needs to consider that the mobility of a genetic element does not translate to motility. Viruses and many microbes in the oceans are non-motile, devoid of appendages for swimming or of the capacity for directional movement and, therefore, can only distribute in a diffusive fashion. It seems like many things would need to align to allow for a chance encounter between a virus and its specific host while floating through the open ocean.
The picture looks different within the sea-ice environment that I described above. In the narrow, brine-filled pores and channels that permeate the ice matrix, microbes and viruses are concentrated, facilitating increased encounter rates and higher potential for infections and genetic interactions compared to seawater. Maybe similar to this concentration effect is the dynamic between humans and influenza or coronaviruses, where infection rates peak in autumn and winter when the colder weather herds us in constrained indoor spaces.
Depending on the time of the year and the air temperatures, the connectedness of the brine space can vary. Colder temperatures in the winter result in further freezing and the decrease of pore spaces, leading to extremely salty, cold and highly concentrated living spaces that can be temporarily sealed off from the surrounding environment. Sounds like an escape room scenario: Trapped with your worst enemy! Viruses are often depicted as selfish killers that inject their genetic material into a host, hijack the host’s resources to build copies of themselves and then induce host cell lysis to free their freshly produced viral progeny. But as with most things in nature, this depiction oversimplifies a much more complex reality. Some viruses choose to linger within their host and to trade their mobile, nomadic lifestyle for a more stable and settled relationship. Instead of going straight into hijack-mode, they establish themselves alongside or within their host’s genome and replicate with the host cell during cell division (Warwick-Dugdale et al., 2019). The lifestyle decision is thought to be driven by the stress level of the host, resource availability in the environment and host density. In unfavorable environmental conditions viruses seem to prefer to linger rather than to kill and move on, using their host as a temporary shelter. In turn, a virus might also protect its host either by suppressing other viruses, or through the genetic information that it carries. For example, some viruses in brines carry genes that can help their hosts to better withstand freezing conditions by changing the composition of their cell envelopes, an adaptation critical for survival in the sea-ice environment (Zhong et al., 2020). It seems like the interactions between these viruses and their hosts could be mutually beneficial and enable their co-existence in a spatially constrained setting, at least temporarily.
Life in Ice
LESSONS (TO BE) LEARNED
It is fascinating how something so tiny, something that is unable to proliferate on its own, can have such a massive impact on ecosystems and play such a central role in the evolutionary history of all life on Earth. If it was not for the pandemic, many of you readers would probably spend very little time thinking about viruses. A lot of the news coverage on viruses over the last years was dominated by attention-grabbing headlines that fed into the narrative of catastrophe. However, this narrative conveys an incomplete and ultimately anthropocentric depiction of the roles of viruses in the environment. These small mobile genetic units of information are in many ways a paradox: From an ecological perspective, viruses hold the power to exploit and kill entire populations, however, this process can free up resources for other organisms to live, making them integral modulators of biodiversity and ecological balance. From an evolutionary perspective, they can be a source of innovation that fosters genomic plasticity and adaptation. Their mobility can thus translate to competitive advantage and enhanced survivability of their hosts. These impacts manifest on evolutionary timescales and may not be immediately measurable for us.
So where am I going with this? Am I trying to find a positive spin to the most recent pandemic? No, not really – the losses and repercussions that many of us have experienced weigh too heavy and the associated emotions are still too vivid. But one should acknowledge that we, as a society, played an essential role in shaping the experienced outcome for our species. Viral outbreaks are natural phenomena, happening billions of times, every second, every day. There is no inherent malicious intent or strategic planning, just a virus seeking means to reproduce. Such outbreaks are typically kept in check by resource availability and host density, but in a hyperconnected world where hosts can travel halfway across the globe in a day the natural controls are losing their grip. Climate change and habitat destruction force species’ movement and reduce living space, meaning that with our actions we are building bridges for otherwise disconnected and widely spread viruses and potential hosts to meet (Carlson et al., 2022). Instead of fear mongering about what viruses can do to us and what other types of horrific diseases are lurking on the horizon, a key point and message to be conveyed is that there is an important interconnectivity of processes, some of which are directly influenced by our actions. While some may argue that they are not (yet) personally experiencing direct effects of climate change on their lives, we certainly all experienced the pandemic (even if to various degrees, and with immense societal disparity). Could such a collective experience create momentum to advocate for change? Could it provide a platform to communicate and explain how closely intertwined the seemingly unrelated processes of the biosphere are and how we are impacting their balance?
In a way, the SARS-CoV-2 virus, this alien form of mobility («alien» because it is different from our typical thinking about what mobility should look like), has brought some momentum and increased our societal plasticity. We adapted to the new stressor, found novel ways to organize our daily lives and work routines, established different means to disseminate information and knowledge and accelerated the development of new vaccines and scientific advancements. These are short-term responses, and whether they can translate into a deeper understanding of the necessary societal changes that need to happen remains to be seen.
My own research is not on human health nor on infection diseases. I have turned to the Arctic to learn about the power of mobility in driving evolution. Sea ice serves as my natural laboratory, and I do not think I will ever get tired of learning about the creative ways that life has found to withstand and adapt to the extremely challenging living conditions. But even up here, so remote and far north, human impacts on the ecosystem are measurable, and most tangible in the rapid decline of sea ice (Rantanen et al., 2022). In climate research, scientists have defined so-called tipping points as «a critical threshold at which a tiny perturbation can qualitatively alter the state or development of a system» (Lenton et al., 2008). I still have hope that we can reach a societal tipping point before reaching further ecosystem and climate tipping points.
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