The oceans inside us

Do I really want to read this? I wondered, scanning the flap of the book. "A bold step forward from Gaia," it said. "The concept of Hypersea will revolutionise the way we perceive and study life on Earth. The ground-breaking new paradigm of Hypersea will stimulate a range of research." Science cannot flourish on such big words, I thought. My eye fell on the preface opening: "We like to think of ourselves as concept people." Mmm. But my suspicions began to fade when I got to the introduction.

Hypersea relates to an important geological event in the early Palaeozoic, more than 400 million years ago - the conquest of the continents by the land plants and their companions. The book explores the adaptive strategies these organisms had to adopt so as to make the transition from the ocean to their new environment and discusses the consequences of the event for the earth's dynamics.

The conquest of land was a giant leap for the biosphere. The oceanic ancestors of land life bathed in a dilute nutrient broth, the ocean water. On land, they met with dryness, at least periodically, while the nutrients were stored in the ground. In response to these harsh conditions, the nutrients had to be mobilised and the aqueous environment internalised, packaged within cells, tissues and specialised conducts. Although the saps of plants and the blood of animals are not seawater, they are similar to it and have analogous biological functions. Hypersea, says the book, is the ocean taken to land. Water and nutrients, from soil and air, must pervade and nurture the maze of branches and leaves sticking up from the ground, while sugars and other energy carriers, generated by the sun in the green parts above descend to the roots. All these treasures are then passed on to the complex food webs dependent on plant life, including the animals, fungi and so on. Efficient recycling and utmost economy are essential, while intimacy is the way to survive.

The tightly interwoven network of life on land offers tremendous opportunities for evolution, especially in the internalised aqueous environment. Every reservoir of host fluids in any individual land organism is a site for speciation; furthermore, defence mechanisms of the host, such as the immune system, provide an exceptionally challenging form of selective pressure for symbionts and parasites. The book abounds with examples of parasites within parasites within parasites within hosts, diverse symbiotic relationships and other kinds of intricate food chains. The authors claim this can only be the tip of the iceberg because we have only begun to explore these internalised ecosystems. In fact, it was the Hypersea concept that made the authors fully aware of this important aspect of land life. They predict that biological diversity on land will turn out to be greater than in the oceans, where the pressure towards internalisation is much less severe.

Anastomosis or the formation of interconnections between the fluid compartments provides opportunities for the spreading of genomes. Thus, "horizontal" gene transfer is likely to be more common, and perhaps much more common, on land than in the sea. Many contemporary health threats have a hypermarine aspect - that is, that body fluid is, to a certain extent, a shared resource. Aids, for example, is regarded as the result of interspecies transfer of Hypersea fluid.

Symbiosis of fungi and algae was an essential prerequisite for the conquest of land. The fungi were specialised in extracting nutrients from the ground and the green algae were good at photosynthesis. Their combination, leading both to lichens and plants, unleashed the evolutionary explosion that paved the way for the animals. While the symbiotic connections in lichens are wellknown, we are usually less aware of the dependence of plants on their fungal companions underground: the nutrient sequestering mycorrhiza. Some plant genes may even be of fungal origin, although the bulk of the genome goes back to algal ancestors.

Among the special characteristics of plants are the rigid cell walls they needed to counter the elevated osmotic pressure in their new fresh-water habitat. These woody sheaths became the elongate conducts which carry the plant sap up and down the stem. The geochemical consequences of this invention are impressive. On land the biomass is many times larger than in the ocean because of the exuberant production of wood; and on geological time scales it led to the massive accumulation of a new type of organic material - coal.

While reading this book, my mood oscillated between admiration and irritation. The Hypersea metaphor made me aware of the supreme eccentricity of land life and it helped me view the ordinary world with new eyes. As such, I am prepared to welcome the idea as a valuable contribution to science. The authors claim, however, that Hypersea is a novel theory. This goes way too far. The comparison of plant saps and body fluids with ocean water rests on analogy and has little or no foundation in the real world. In fact, the authors admit that they are very different chemically. This does not prevent them carrying the analogy several steps further: they consider vertical transport of plant sap as hypermarine ocean upwelling, lateral transport by underground roots and fungi as hypermarine ocean currents, and natural syrupy concentrates on plant surfaces as hypermarine evaporitic sediments. We have known since the days of Kant that scientific arguments must never be founded on analogies, but the authors are dead serious about these poetic digressions.

There is more I dislike. The Hypersea concept excludes the descendants of the first, microbial, wave of land exploitation, probably dating back several billions of years and ignores the important role these humble predecessors may have played in getting the Hypersea conquest established. Relics of this original land biota still occur in hostile places that Hypersea cannot reach - in beach sands, salt ponds and hot springs. Despite their humble appearances, however, they harbour the full plethora of metabolism of the biosphere in less than a centimetre and are capable of extracting and subsequently recycling all the essential nutrients from ground, water and air. Viewed from this standpoint, plants and animals did little more than providing an amplification of some pre-existing microbial faculties, notably photosynthesis and aerobic respiration, while the fungal part of Hypersea vastly improved on the nutrient retrieval of the bacteria. Even today, the Hypersea system still must rely on the ancient bacterial rank and file for anaerobic metabolism, essential as it is in the recycling of foodstuff. Thus, in stead of replacing the older settler communities, Hypersea had to worm its way into their organisation, and replace some of their component parts with its own more efficient functions.

I also tend to believe that the fungi were born in microbial communities on land, rather than in the ocean as Hypersea would have it. The early microbial systems must have been perfectly capable of retrieving their nutrients from the underlying rocks and today this faculty remains the specialty par excellence of the fungi. One may then envisage how the fungi were wrought inside the dense microbial tissues in a symbiotic event that included the specialist mining bacteria, while later on associations with green algae led to the lichens and plants.

Hypersea is a mixed bag. It abounds with interesting observations and fascinating details, and the authors convey a genuine feeling of naive enthusiasm about their idea. It is also chaotic, very repetitive and poorly organised. Especially in the middle part of the book I was often overwhelmed with examples and lost track of the argument, even though the glossary and index were extensive.

Shall we bury Hypersea? In its present form the concept is too fuzzy and pretentious to be very useful. But I wish we could hang on to the precious jewel this book has to offer: a new look at the bizarre intricacies of our everyday surroundings. Please don't give up, you concept people!

Peter Westbroek is head of the geobiochemistry unit, University of Leiden, The Netherlands.