If there are forms of life on Earth today with a biochemistry not like our own, how would we even know it?

Carol Cleland is a professor of philosophy at the University of Colorado, Boulder, and a member of the NASA Astrobiology Institute. In the third of our series of "gedanken" thought experiments, Cleland explores the possibility that Earth could be host to an undiscovered "shadow biosphere" of alternative forms of microbial life.

When scientists speculate about life as we don't know it, they typically have in mind extraterrestrial life. The possibility that the present day Earth might harbor an alternative form of life is rarely considered.

Given that biologists have yet to encounter an alternative form of Earth life, this may seem reasonable. Indeed, if there were alternative forms of life analogous to plants and animals on Earth, we undoubtedly would have stumbled upon them by now.

However, the situation is quite different for microbes, which are too small to be seen with the unaided eye. Could the contemporary Earth be host to "shadow microbes" -- undiscovered alternative forms of microbial life?

Philosophers and scientists traditionally focus upon two characteristics that distinguish a living system from a nonliving system. First, the capacity of a system to maintain itself as self-organized unit against both internal and external perturbations. And second, the ability to reproduce and transmit to its descendants adaptive heritable modifications.

Molecular biology provides an account of how our familiar Earth life realizes these abstract functional properties in a concrete physical system. Life as we know it on Earth today is based upon a complex cooperative arrangement between proteins and nucleic acids.

Proteins supply the bulk of the structural material for building bodies, as well as the catalytic material for powering and maintaining them. Nucleic acids store the hereditary information required for reproduction and for synthesizing the enormous quantity and variety of proteins required by an organism during its life span.

The crucial process of coordinating these functions-of translating the hereditary information stored in nucleic acids into proteins for use in growth, maintenance, and repair-is handled by ribosomes, minuscule but highly complex molecular devices composed of both protein and nucleic acid (RNA).

Admittedly, we don't know how different life could be from life as we know it, because we don't know all the ways in which a physical system could realize the functions attributed to life. Moreover, we can't rule out the possibility that the most important characteristics of life have yet to be discovered. The functions traditionally attributed to life may be little more than symptoms of more fundamental but as yet unknown properties.

Some of the molecular building blocks of proteins and nucleic acids could have been modestly different without affecting their biological functionality. Although abiotic processes produce over 100 amino acids of mixed chirality (molecular "handedness"), familiar Earth life constructs its proteins from the same 20 amino acids, and they all have the same "left-handed" chirality. From a molecular and biochemical perspective, this is mysterious.

Proteins synthesized in the laboratory from combinations of alternative amino acids or amino acids of the opposite chirality fold into complex three-dimensional structures having structural and catalytic potential. They undoubtedly would be functional in appropriate environments.

Furthermore, with the exception of RNA viruses, all life on Earth utilizes DNA to store its hereditary information. Four bases -- adenine, thymine, guanine, and cytosine -- are arranged in two mutually exclusive pairs to encode the information. But the molecular building blocks of DNA could have been different. As Steve Benner and his co-workers have demonstrated, double-stranded DNA can accommodate at least 12 bases arranged in six mutually exclusive pairs.

Hereditary information is encoded on nucleic acids by means of a unique but somewhat redundant correspondence between amino acids and triplets of bases (codons). But there is little reason to suppose that some codons couldn't have been paired with different amino acids. It has been argued that a triplet coding scheme is the most efficient for 4 bases and 20 amino acids. It is unlikely, however, that the same would be true for a form of life using a different number of bases or amino acids.

So why does life as we know it on Earth today use its particular combinations of molecular building blocks? The best explanation is that they are the result of conditions on the early Earth. This is true not only for proteins and nucleic acids, but also for ribosomes. Because they physically realize the translation of hereditary information into functioning, self-maintaining organisms, ribosomes lie at the very heart of the molecular architecture of familiar life.

Their unique characteristics are almost certainly the product of historical contingencies. So it is unlikely that the ribosomes found in the cells of familiar life represent the only possibility for translating hereditary information stored on nucleic acids into proteins, let alone the original mechanism utilized by the first proto-cells. Had circumstances on the early Earth been different, familiar life would also have been different.

This opens up a provocative possibility. It is commonly assumed that life originated only once on Earth. But if the emergence of life is highly probable under certain physical and chemical circumstances that were present on the early Earth, then there could have been multiple cradles of life. There must have been natural variations in the collections of organic molecules available in different regions on the early Earth. Assuming that life did originate on Earth and was not transported here from elsewhere, then it is unlikely that the first forms of Earth life were all built from exactly the same molecular building blocks.

While many biologists and biochemists are willing to concede that the first proto-organisms may have used different molecules, few are willing to take the next step and seriously entertain the possibility that their microbial descendents may still be with us today. Three reasons are commonly cited. First, any variations in the earliest forms of life would have been combined by lateral gene transfer into a single form of life.

Second, our ancestors would have eliminated other life forms long ago in the ruthless Darwinian competition for vital resources. And third, if alternative forms of life existed, we would have discovered them, or at the very least stumbled upon signs of them. But as my colleague Shelley Copley and I have argued, none of these reasons stand up under close scrutiny.

"Lateral" gene transfer is when genes are transferred from the genome of one microbe to that of another, rather than being transferred "horizontally," from parent to child. Lateral gene transfer is very common among microbes, occurring among widely different varieties, including those from the different domains of life (Archaea, (Eu)bacteria, and unicellular Eukaryia).

Not unsurprisingly, lateral gene transfer is thought to have played a central role in microbial evolution. Carl Woese speculates that the earliest proto-cells engaged exclusively in lateral gene transfer. He contends this process would have combined any alternative forms of primitive life into a single homogenous pool of proto-cells, from which life as we know it today eventually emerged.

The problem with this scenario is that lateral gene transfer (as we know it today) is possible only for microbes that share the same core molecular machinery for replication, transcription, and translation. All known microbes share this machinery, which is why they can engage in lateral gene transfer. But no microbe from any of the three domains could incorporate genes from even a modestly different form of life - one that utilized bases differing in either identity or number, for instance - into its genome. Even supposing that such an event were to occur, the gene could not be replicated or used to make protein.

Exchanges between Woese's proto-cells are supposed to have occurred before the machinery for replication, transcription, and translation was available. But still, it is difficult to see how the complex cooperative arrangement between proteins and nucleic acids that characterizes life as we know it today could emerge from a disorganized exchange of primitive biomolecules such as polypeptides and oligonucleotides.

Even supposing that it could, it is unlikely that such a process would produce a single, planet-wide pool of homogenous proto-cells. Earth is a big place, and geographical isolation would inevitably occur, just as it does today, producing local pools of proto-cells differing in some of their basic molecular building blocks.

Rather than a single homogenous community of cells, lateral gene transfer is likely to yield a variety of isolated homogenous communities, several of which could have independently made the transition to more sophisticated forms of microbial life or, for that matter, still exist as remnants of the first life on Earth.

The point is that our current knowledge of lateral gene transfer does not provide support for the claim that there couldn't be alternative forms of microbial life on the Earth today.

It is sometimes maintained that our form of life is so robust and aggressive that no other form of life could survive competition with it. This objection does not, however, bear up. Microbial communities are highly organized systems that modify their environments in significant ways, creating stable ecological niches. The diversity of such communities is staggering.

They typically contain microbes from all three domains of life, and the number of different species within a given domain is enormous. Some species are present in very small numbers. Being a rare microbe is not an evolutionary disadvantage, however, because rare microbes occupy different ecological niches than common microbes, producing or utilizing material that is utilized, produced or ignored by other varieties of microbe.

There is little reason to suppose that microbial descendents of an alternative origin of life couldn't participate with familiar microbes in a community, even supposing that they were present in very small numbers.

But if they were somehow disadvantaged in the competition for vital resources, an alternative form of microbial life might have evolved in such a way as to essentially remove itself from competition with familiar life. Natural selection could have favored the survival of those that were most different from familiar life in their basic molecular building blocks, and so familiar life would have found them less nutritious.

Alternatively, a different form of microbial life might have adapted to environments that are less hospitable to familiar life, such as extremely dry deserts.

In other words, it just isn't obvious that an alternative form of microbial life couldn't evolve in such a way as to survive competition with familiar microbes.

This brings us to what is perhaps the most scientifically compelling objection: That if there were an alternative form of microbial life on Earth, we would have found it by now, or at least encountered signs of it, using the sophisticated tools available to contemporary microbiologists.

The primary tools used for exploring the microbial world are microscopy, cultivation, and PCR amplification of rRNA gene sequences. Microscopy is of limited utility. The phenomenon of convergent evolution has taught us that superficial similarities in body structure can be very misleading. Archaean microbes provide a good example. Under a microscope they look pretty much like Eubacteria, and indeed until fairly recently both were classified simply as "bacteria".

Both lack membrane-enclosed intracellular structures, and thus differ from unicellular Eukarya, which have membrane-enclosed intracellular structures like a nucleus. This striking difference lies behind the infamous prokaryote-eukaryote distinction, which until fairly recently provided the central justification for grouping all prokaryotic microbes together under a single kingdom ("Bacteria"). Yet we now know that there are greater genetic and biochemical differences between the Archaea and the Eubacteria than there are between the Archaea and the Eukarya.

This discovery revolutionized biological taxonomy, replacing the traditional five kingdoms of life (Animalia, Plantae, Fungi, Protoctista, Bacteria) with three domains of life (Eukarya, Eubacteria, Archaea). So it would be a mistake to conclude that any microbe that looks like a familiar form of life under a microscope actually is a familiar form of life.

Our most extensive knowledge of individual microbes has been achieved through cultivation. Cultivating a microbe produces large quantities of identical microbes, allowing microbiologists to perform extensive analyses of that microbe's structural, enzymatic, and genetic material. Our ability to culture microbes is quite limited, however. It is estimated that less than 1 percent of what we can see under a microscope has been cultured.

The problem is that microbes thrive under very different physical and chemical conditions - different pressures, temperatures, pH, and so on. They exploit a wide diversity of energy and nutrient resources. It is difficult to identify, let alone replicate, these complex conditions in a laboratory setting. The situation is even worse for an alternative form of microbial life, because it is more likely to require unanticipated chemical and physical growth conditions.

So just because no one has discovered an alternative form of microbial life growing in a petri dish, we can't conclude that such microbes don't exist.

Polymerase chain reaction (PCR) amplification of ribosomal RNA genes is the most powerful tool currently available for identifying difficult-to-culture microbes in environmental samples. There are two features of PCR amplification that make it a very poor tool for detecting alternative forms of microbial life. It amplifies ribosomal RNA (rRNA) genes, so it wouldn't allow us to detect a form of life that lacked ribosomes. PCR amplification also requires the use of universal primers (small pieces of synthetic nucleic acid) from one of the three domains of life.

Even supposing that an alternative form of microbial life had ribosomes, which seems unlikely, its rRNA would almost certainly be too different from that of the three domains of familiar life to be amplified by PCR. In fact, any microbe whose rRNA genes could be amplified by PCR must be a familiar form of life! So our failure to detect alternative forms of microbial life in environmental samples by means of PCR does not provide us with a good reason for believing that they do not exist.

This brings us to the last objection. Life invariably modifies its environment, extracting energy, building structures, and producing waste products. If an alternative form of microbial life existed, perhaps we wouldn't have identified it yet but surely we would have encountered its traces -- the "shadows" that it would cast upon its environment.

Yet it would be difficult to recognize traces of an alternative form of microbial life against the "background noise" produced by familiar microbes. Also, when faced with a perplexing, seemingly biological trace, the default assumption is that it was produced either by familiar life or by non-biological processes. The possibility that it represents an alternative form of microbial life is never seriously entertained. The assumption that there is only one form of life present on Earth today is part of the paradigm of modern biology.

Thomas Kuhn stated that the vast majority of scientific research is conducted within the confines of a paradigm. Paradigms include not only theories but also methods, instruments, concrete examples, sanctioned texts, and, most importantly for our purposes, subsidiary assumptions. They are invaluable tools for scientific research, facilitating the construction of hypotheses, design of experiments, and interpretation of results.

According to Kuhn, however, paradigms may also hinder the exploration of nature, blinding researchers to important possibilities by discouraging certain avenues of investigation and biasing the ways in which data are interpreted.

As a consequence, important scientific discoveries may be delayed for years. Kuhn used examples from astronomy to illustrate how paradigms can blind scientists to new discoveries. Similar cases can be found in biology, such as the discovery of Archaea, a new variety of familiar microbial life that revolutionized biological taxonomy.

In hindsight, it is clear that there were signs that some prokaryotes are fundamentally different from others, despite their remarkable similarities in cell morphology. But because biologists were working under the prokaryote-eukaryote paradigm, which used cellular morphology as the guiding principle for understanding taxonomic relations, these signs went unrecognized.

Indeed, what are now understood to be telling chemical differences in the membranes of Archaea and Eubacteria were interpreted as mere adaptations of familiar "bacteria" to extreme environments. Microbiologists had unwittingly stumbled upon a new kind of microbe, but failed to recognize it because they were working under the prokaryote-eukaryote paradigm, which denied that such microorganisms exist.

The lesson should be clear. Because microbiologists are working under a paradigm that says there is only one form of life on Earth today, it is unlikely that they would recognize the significance of traces of an alternative form of microbial life even if they encountered them.

While we don't know how different life could be from life as we know it, there are good reasons for thinking that life on Earth could have been at least modestly different in its molecular architecture and building blocks. A dedicated search for shadow microbes ought to be seriously considered. The obvious place to begin is with known puzzling phenomena, such as desert varnish, that are difficult to explain in terms of familiar life and yet also difficult to explain in terms of abiotic processes.

The discovery of a shadow microbial biosphere would be philosophically and scientifically important. It is clear that familiar Earth life has a common origin, and hence represents a single example of life. Logically speaking, one cannot generalize on the basis of a single example. If we are to achieve a satisfactory understanding of the general nature of life, we need examples of unfamiliar forms of life.

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