More Than Meets the Eye Earth’S Real Biodiversity Is Invisible, Whether We Like It Or Not

24.9 commentary 804 MH 18/6/04 5:44 pm Page 804

commentary More than meets the eye Earth’s real biodiversity is invisible, whether we like it or not.

Microsporidia are now thought to be highly Sean Nee divergent fungi — highly divergent indeed! The world has creatures that ‘breathe’ iron Metabolic diversity. Life requires energy. and uranium, using these elements in the Visible life exploits only one of the many same way as we use oxygen. Others thrive in possible metabolisms to get energy, taking the equivalents of hot sulphuric acid or electrons from organic carbon compounds floor stripper, and others again live in solid and giving them to oxygen — breathing rock. In terms of biomass, the single most oxygen with which to burn food. This is abundant form of life on Earth is ocean- mainly how animals and plants fuel them- RAMOUNT/THE KOBAL COLLECTION RAMOUNT/THE KOBAL

sediment-dwelling bacteria and, numerically, selves,although plants,of course,use light to PA the most abundant life-forms in the ocean manufacture their own food.In comparison, are viruses. We are still at the very beginning the invisible microbial world has a far of a golden age of biodiversity discovery, greater metabolic repertoire. As I have driven largely by the advances in molecular mentioned, there are creatures that ‘breathe’ biology and a new open-mindedness about metals, using them as electron acceptors; where life might be found. But for this others use metals as electron donors — they golden age to be as widely appreciated as it ‘burn’ metals. A quarter of a century ago it should, our view of the natural world must was predicted, on energetic grounds, that a change — as radically as did our view of creature should exist that burns ammonia the cosmos when we began looking at it with nitrite for energy (who says biology is with technologies that allowed us to see not a predictive science?).Such bacteria were more than can be seen with the naked eye. recently discovered1. For all of the marvels in biodiversity’s Visible life can use one inorganic energy new bestiary are invisible. As many pundits source — light — to manufacture organic have pointed out (usually in the restricted compounds,but invisible life can also exploit context of bacterial diversity), by any crit- Mr Spock – unemotional role model. chemical energy. Chemical energy almost erion — biomass or numbers of individuals certainly fuelled the first creatures that lived — life on Earth is microscopic. It is the new phyla are all or partly microscopic (numeri- on Earth, and microbes that exploit a large generation of explorers of this ‘invisible’ cally, four out of five animals are micro- variety of such sources provide the basis for world who are transforming our world- scopic nematodes). But a new view of life’s the rich communities that thrive in the pitch view beyond recognition. Yet a six-article interrelationships has emerged from darkness around hydrothermal vents on the Insight special on biodiversity in this jour- molecular data, in particular from the DNA sea floor — which were unknown to us until nal in May 2000 scarcely mentioned any- sequences of genes that encode important a quarter of a century ago. thing that could not be seen unaided. RNA molecules found in all organisms. The major biogeochemical cycles on This is not to say that the papers were not On the tree of life (see opposite) based on which we depend were in place three billion a fair reflection of what biodiversity science analyses of this ‘small-subunit ribosomal years ago, long before the appearance of is at the moment — that is, firmly fixated on RNA’ (ssRNA), visible life consists of barely visible life, and are today maintained by the the visible world. And I am not suggesting noticeable twigs. This should not be ‘invisibles’ and their vast range of metabo- that senior commentators on biodiversity, surprising — invisible life had at least three lisms. The persistence of life on Earth such as Robert M. May and Edward O. billion years to diversify and explore evolu- depends on the endless recycling of essential Wilson, have been blind to the invisible. But tionary space before the ‘visibles’ arrived. elements such as sulphur, iron and nitrogen it is now time for biologists — by whom I The branch lengths in this figure are through their various forms. Thanks to mean people who think of themselves as informative about diversity in terms macroscopic life, ecosystems are more biologists, zoologists, botanists and ecolo- of degree of divergence, and not just in the productive and nutrient cycling is more gists — to cease presenting to their students RNA genes used to construct the tree. rapid; animals and plants are good at and the public a perspective of life on Earth Creatures that are distantly related according churning things up. But the ‘visibles’ have that is so biased towards the visible. This will to their RNA genes are genetically divergent introduced no qualitatively new features to not be easy. The first part of the challenge is in many other respects. Consider the global ecology. accepting that the contribution of visible life microsporidia, classically placed as a long Environmental diversity. Our awareness to biodiversity is very small indeed. branch at the ‘base’ of the Eukarya, one of the astonishing range of environments of the three main domains of life. These in which microbial life can thrive continues Types of diversity are remarkable intracellular parasites; to expand. The superheated, pressurized Phylogenetic diversity. The old ‘five king- their spores are wrapped in what is essen- environment of an autoclave, used for doms’ view of the relationships between tially a flexible hypodermic needle, and sterilization at 120 °C, would be ideal for the organisms gave prominence to macroscopic they infect a cell by piercing it and injecting growth of‘strain 121’,an ‘iron-breathing’crea- creatures, with three of the kingdoms being themselves.In humans they cause diarrhoea. ture from a hydrothermal vent,which survives animals, plants and fungi. But even under They are almost certainly misplaced in this at even 130 °C.The greatest extremes of acidity, this classification, the invisible world asserts tree as a result of a well-known artefact alkalinity,salinity and so on are not so extreme itself. The phylogenetic rank just below called ‘long branch attraction’, whereby as to preclude invisible life. The Dead Sea is kingdom is phylum, and 40% of animal very long branches get grouped together. very much alive — it just doesn’t contain fish.

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Although representatives of the bacteria microbiology. To update our view of life on biodiversity would not even recognize that and archaea are the most famous Earth, biologists need to overcome the gulf this is a highly important journal for them. extremophiles, microbial eukaryotes that between microbiology and biology that first And even when discoveries are published in occupy this stage are now also being discov- arose about 150 years ago, and which retains the high-profile literature, as they frequently ered. Life in the Rio Tinto (river of fire) much of its original character. Charles are, biodiversity enthusiasts are unlikely to in Spain — which is metal-contaminated Darwin voyaged the high seas, dining at the register such titles as “An archaeal iron- and as acidic as your stomach — is domin- captain’s table, before retiring to his country oxidizing extreme acidophile important in ated by an extremely diverse array of them. house to develop his various ideas. Louis acid mine drainage”2 — which reports the A combination of the same molecular Pasteur, on the other hand, was hired as a discovery of creatures that are surely at least as techniques used to study bacterial diversity consultant to the alcohol industry and astonishing as “Striped rabbits in Southeast in nature, as well as a willingness to look for discovered organisms that can live without Asia”3.Ifbiologists want to keep up with this them in supposedly inhospitable places, oxygen. He experimented with heat treat- new golden age of biodiversity study, then is revolutionizing our understanding of ments to prolong product shelf-life and there is no choice but to learn or relearn our eukaryotic diversity, just as it is doing for developed vaccines to prolong human life. basic chemistry,redox reactions in particular. bacterial diversity. Darwin was a biologist, Pasteur a micro- Morphological diversity. Visible life wins Emotional bias hands down in this category, although We are sentimental about visible nature yet the invisible world puts up a good show Bacteria utterly self-centred about the invisible — with diatoms. Colours, noise, outlandish Archaea simply happy with it if it is useful, such as behaviour, emotion and consciousness — bakers’ yeast, or bent on its extermination these must count for a lot. But none of it is if it is unpleasant or harmful (for example, really necessary for life on Earth, unlike the a yeast infection). And, if it is not obviously activities of invisible organisms, which important to us in one way or another, we terraformed the planet for visible organisms, do not even give it a thought. As May creating and maintaining the atmosphere has said4:“As one moves down the size and nutrient cycles on which we depend. spectrum of organisms, from the romantic Even the oxygen content of the atmos- large mammals and birds, through non- phere depends entirely on the invisible descript small arthropods, on down to

world of phytoplankton. Although roughly AnimalsFungi protozoan, bacterial and viral species, not half of the planet’s oxygen is produced by only does concern for diversity and conser- terrestrial plants, this is mostly used up in Plants vation fall away, it even changes sign.” terrestrial respiration. The primary reason As biologists, we must recognize this why the oxygen content of the atmosphere emotional bias and try to control it, like Mr does not dwindle to zero is because of the Spock. Honesty to ourselves in considering rain of dead and dying oceanic microbes what life is — and in presenting an honest from the surface waters to the ocean floor. picture to students and the public — Buried in the sediments, the oxygen they Eukarya demands it. Consider ‘syntrophy’.This is the produced is not used up in their decomposi- dominant ecological relationship in worlds tion, resulting in a net gain of oxygen by the Biodiversity through a molecular lens. This without oxygen5 — such as sediments and atmosphere and oceans. It is a measure of scheme is based on ssRNA gene-sequence data, your gut — and is the phenomenon whereby how recently we have really started to get to and shows the relationships of organisms in the the metabolic waste product of one species grips with the microbial world that the most three main domains of life — Bacteria, Archaea is the primary food or energy source of abundant constituent of the plankton, and Eukarya (creatures with cell(s) like our another (there are stricter definitions). The Prochlorococcus, was discovered less than 20 own). Visible organisms are found among the syntrophic networks that take in organic years ago. For emotional reasons, we attach plants, animals and fungi. Yet not only are these material provided by the oxygenated worlds great significance to the morphological groups just twigs on the tree of life, but many of and output the final waste products of dimension of diversity — biologists are their members are invisible as well. carbon dioxide and water can be complex. largely attracted to the subject in the first But syntrophy is not mentioned in any place by this emotion. biologist. Microbiologists are employed major ecological textbook. Ecology students by the wine and sewage industries; biologists carry around inside their guts highly diverse Departmental affiliations go to wine tastings and discuss biodiversity ecologies, and this is simply never even A reflection of biologists’ obsession with and conservation in between using the mentioned. This neglect of the invisible the visible world can be seen in the depart- bathroom. In the index to the standard world is no longer any more acceptable than, mental affiliations of the explorers of the microbiology textbook (Brock Biology of say, teaching astronomy but ignoring the invisible world. With notable exceptions, Microorganisms) you will find entries such as existence of galaxies beyond the Milky Way, these are rarely ‘biology’ or ‘zoology’. ‘jock itch’,‘sewage fungus’ and ‘Swiss cheese’ or teaching physics while refusing to discuss Rather, more commonly, they are ‘geology’, — these are not the sorts of topics that turn anything smaller than a pin head. ■ ‘biotechnology’ or ‘oceanography’, and on biology students. One challenge for Sean Nee is in the Ashworth Laboratories, even ‘civil engineering’, ‘planetary science’ biologists is to find ways of making sewage University of Edinburgh, West Mains Road, and ‘astrobiology’. And astonishing new fungus palatable to our students and the Edinburgh EH9 3JT, UK. discoveries that challenge our views on the general public. e-mail: [email protected] nature of life are more likely to be Microbiologists do not even give a ‘biodi- 1. Strous, M. et al. Nature 400, 446–449 (1999). announced at a Geological Society meeting versity’label to their studies — they call them 2. Edwards, K. J., Bond, P. L., Gihring, T. M. & Banfield, J. F. Science 287, 1796–1799 (2000). than a conference seemingly devoted to ‘environmental microbiology’.A major jour- 3. Surridge, A., Timmins, R. J., Hewitt, G. M. & Bell, D. J. Nature biodiversity. nal publishing fundamental discoveries in 400, 726 (1999). 4. May, R. M. Phil. Trans. R. Soc. Lond. B 330, 293–304 (1990). Many of the explorers of the realm of the this area is Applied and Environmental 5. Fenchel, T. & Finlay, B. J. Ecology and Evolution in Anoxic Worlds invisible are, of course, in departments of Microbiology.Most biologists interested in (Oxford Univ. Press, 1995).