Intraterrestrials Discovering the Strangest Life on Earth

Some of the more exciting developments in biology in recent decades have been in geomicrobiology. Whole new branches of microbial life have been discovered hiding out of sight inside the rocks and sediments making up our planet, forming a veritable subsurface biosphere. Having just reviewed Deep Life, which charted the history of these discoveries through the career of the late geoscientist Tullis C. Onstott, I now turn to Karen G. Lloyd's Intraterrestrials. This thought-provoking book provides a broader take on the subject and shows how these microbes challenge our understanding of life.

Intraterrestrials is a compact book organised into three parts, though the material really boils down to two approaches. The three chapters in part 1 give a general introduction to the subsurface environment and how its microbial life is studied. How do nutrients move around in Earth's crust, and where do they come from? How do you retrieve these microbes? How do you study them? What stands out in this first part is Lloyd's excellent metaphors and analogies to explain these concepts and answer questions. How is the subsurface biosphere organised? As localised hotspots: "It's as if there are millions of little low-powered suns distributed throughout Earth's crust, each one with its own tiny orbit of a subsurface ecosystem" (p. 18). Why are scientists so interested in hydrothermal vents at the bottom of the ocean? Because they are "like natural sampling ports for deep subsurface fluids" (p. 34). And why was it initially so hard to get good estimates of the number of species living underground? Because early DNA sequencing technology was slow, so we could only look at a limited number of sequences. "Try guessing the total number of species in a rainforest from a list that only includes two types of trees, one monkey, and one frog. It's a statistician's nightmare" (p. 44).

The eight chapters in parts 2 and 3 form the second prong to this book's approach and explore why the subsurface biosphere matters and how it challenges biology. This, in my opinion, is where the book really gets going. Two obvious ways in which intraterrestrials are changing basic notions about biology are that the tree of life is much bigger than we thought, and the conditions that can support life are much broader than we thought. If you keep up with microbiology, you know all this. Instead, there are three other areas where Lloyd pushes this book into thought-provoking territory and shows how studying these microbes questions basic tenets of biology.

The first has to do with thermodynamics. One of life's most essential functions is moving energy around: it mixes up chemicals, which releases energy, and then captures this energy to power life's processes. This is where Lloyd goes into some excellent explanations on thermodynamics. Without going into the details, the gist is that by looking at life through a thermodynamics lens, you understand that where there is excess energy that can be liberated through chemical reactions, life can be supported. Animals use oxygen for this, but there is nothing against using other chemicals. Respiration in the broad sense of the word is about much more than just oxygen, and intraterrestrials can "breathe" all sorts of other substances; they need not even be gaseous. By examining the basics, you can both understand and predict where else in the thermodynamic space of possibilities life can be supported, even if the energy margins are slimmer.

Second is the ultraslow lifestyle of intraterrestrials and the question of how this evolved. We readily assume that microbes grow very fast, but is that because those are the only ones we choose to study? We are limited by our lifespan and the short funding cycles in science, so "the necessity of laboratory expediency may have given us the incorrect impression that most microbial life on Earth grows fast" (p. 140). Intraterrestrials rarely divide into daughter cells; can that be an adaptation? Lloyd argues yes: it requires too many physiological changes to be accidental, and we do not find faster-growing forms in other environments; they live exclusively deep underground. Can evolution even operate if you do not produce offspring? This is where we need to recalibrate our perspective, for, to paraphrase Lloyd, we are like the adult mayfly who lives just one day, struggling to comprehend how an overwintering tree can be dormant for months on end. Intraterrestrials only produce offspring very occasionally. But what are they waiting for? Could it be "for wake-up cues we don't recognize because our lives are too short to see them?" (p. 149). Intriguingly, Lloyd suggests that geological events such as earthquakes, landslides, or volcanic eruptions could shift intraterrestrials around and expose them to new food sources, coaxing them out of dormancy after millennia. This is where she coins a wonderful term of her own: if we call heat-loving microbes thermophiles maybe we should call these long-lived, time-loving microbes aeonophiles. "Geological events may be as consequential to an aeonophile as daybreak is to a songbird" (p. 156).

Third and final is what intraterrestrials could reveal about the origin of life. Where and how did life start? Lloyd favours deep-sea hydrothermal vents as providing both the place and the chemical conditions suitable to early life. When did life originate? Even the oldest rocks seem to contain microfossils and chemical signals, suggesting that life has been around for at least 3.85 billion years. They might even offer an answer as to the why of life's origin. If life creates ordered structures that push a system out of thermodynamic equilibrium, perhaps intraterrestrials have found a novel way of doing so by spreading it out over very long timescales. I am not sure I am explaining this very well, and I admit that this section of the book went somewhat over my head, taking, as it does, a whirlwind tour through non-equilibrium thermodynamics, entropy, dissipative structures, and autocatalytic systems and draws on, amongst others, Schneider and Sagan's book Into the Cool.

Compared to Onstott's Deep Life, Intraterrestrials is a leaner and meaner beast. All excess fat has been trimmed from this manuscript, and the writing is focused and to the point: there is no massive endnote section, just some footnotes scattered throughout; the few autobiographical asides serve to flavour the book but do not dominate it. In less than half the number of pages, Intraterrestrials manages to interrogate why studying underground microbes is relevant and throws out some thought-provoking ideas. With all due respect to the late Onstott, but for those wishing to venture into the underworld, I suggest you start here.