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Nigel Goldenfeld and Carl Woese

One of the most fundamental patterns ofscientific discovery is the revolution inthought that accompanies a new body ofdata. Satellite-based astronomy has, dur-ing the past decade, overthrown our mostcherished ideas of cosmology, especiallythose relating to the size, dynamics andcomposition of the Universe.

Similarly, the convergence of fresh theo-retical ideas in evolution and the comingavalanche of genomic data will profoundlyalter our understanding of the biosphere and is likely to lead to revision of conceptssuch as species, organism and evolution.

Here we explain why we foresee such a dra-matic transformation, and why we believethe molecular reductionism that dominatedtwentieth-century biology will be super-seded by an interdisciplinary approach thatembraces collective phenomena.

The place to start is horizontal gene trans-fer (HGT), the non-genealogical transferof genetic material from one organism toanother such as from one bacterium toanother or from viruses to bacteria. Amongmicrobes, HGT is pervasive and powerful for example, in accelerating the spread ofantibiotic resistance. Owing to HGT, it is not

a good approximation to regard microbes asorganisms dominated by individual char-acteristics. In fact, their communicationsby genetic or quorum-sensing channelsindicate that microbial behaviour must beunderstood as predominantly cooperative.

In the wild, microbes form communities,invade biochemical niches and partake inbiogeochemical cycles. The available stud-ies strongly indicate that microbes absorband discard genes as needed, in responseto their environment. Rather than discretegenomes, we see a continuum of genomicpossibilities, which casts doubt on the

validity of the concept of a species whenextended into the microbial realm. The use-lessness of the species concept is inherent inthe recent forays into metagenomics thestudy of genomes recovered from naturalsamples as opposed to clonal cultures. Forexample, studies of the spatial distributionof rhodopsin genes in marine microbessuggest such genes are cosmopolitan, wan-dering among bacteria (or archaea) as envi-ronmental pressures dictate.

Equally exciting is the realization thatviruses have a fundamental role in the bio-sphere, in both immediate and long-term

evolutionary senses. Recent work suggeststhat viruses are an important repository and

memory of a communitys genetic informa-tion, contributing to the systems evolution-ary dynamics and stability. This is hintedat, for example, by prophage induction, inwhich viruses latent in cells can becomeactivated by environmental influences.The ensuing destruction of the cell and viralreplication is a potent mechanism for thedispersal of host and viral genes.

It is becoming clear that microorganismshave a remarkable ability to reconstructtheir genomes in the face of dire environ-mental stresses, and that in some cases theircollective interactions with viruses may becrucial to this. In such a situation, how validis the very concept of an organism in isola-tion? It seems that there is a continuity ofenergy flux and informational transfer fromthe genome up through cells, community,virosphere and environment. We wouldgo so far as to suggest that a defining char-acteristic of life is the strong dependencyon flux from the environment be it of

energy, chemicals, metabolites or genes.Nowhere are the implications of col-lective phenomena, mediated by HGT, sopervasive and important as in evolution.A computer scientist might term the cellstranslational apparatus (used to convertgenetic information to proteins) an oper-ating system, by which all innovation iscommunicated and realized. The funda-mental role of translation, represented inparticular by the genetic code, is shownby the clearly documented optimizationof the code. Its special role in any form oflife leads to the striking prediction that

early life evolved in a lamarckian way,with vertical descent marginalized by the

more powerful early forms of HGT.Refinement through the horizontal shar-

ing of genetic innovations would have trig-gered an explosion of genetic novelty, untilthe level of complexity required a transi-tion to the current era of vertical evolution.Thus, we regard as regrettable the conven-tional concatenation of Darwins name withevolution, because other modalities mustalso be considered.

This is an extraordinary time for biology,because the perspective we have indicatedplaces biology within a context that mustnecessarily engage other disciplines morestrongly aware of the importance of col-lective phenomena. Questions suggested

by the generic energy, information andgene flows to which we have alluded willprobably require resolution in the spirit ofstatistical mechanics and dynamical sys-tems theory. In time, the current approachof post-hoc modelling will be replaced byinterplay between quantitative predictionand experimental test, nowadays morecharacteristic of the physical sciences.

Sometimes, language expresses ignorancerather than knowledge, as in the case of theword prokaryote, now superseded by theterms archaea and bacteria. We foresee thatin biology, new concepts will require a new

language, grounded in mathematics and thediscoveries emerging from the data we havehighlighted. During an earlier revolution,Antoine Lavoisier observed that scientificprogress, like evolution, must overcome achallenge of communication: We cannotimprove the language of any science withoutat the same time improving the science itself;neither can we, on the other hand, improvea science without improving the language ornomenclature which belongs to it. Biologyis about to meet this challenge. Nigel Goldenfeld is in the Department of

Physics and Institute for Genomic Biology,

University of Illinois at Urbana-Champaign,1110 West Green Street, Urbana, Illinois

61801, USA. Carl Woese is in the

Department of Microbiology and Institute

for Genomic Biology, 601 South Goodwin

Avenue, Urbana, Illinois 61801, USA.

FURTHER READINGFrigaard, N., Martinez, A., Mincer, T. & DeLong, E. Nature439,847850 (2006).Sullivan, M. et al. PLoS Biol.4,e234 (2006).Pedulla, M. et al. Cell113, 171182 (2003).Vetsigian, K., Woese, C. & Goldenfeld, N. Proc. Natl Acad.Sci. USA103, 1069610701 (2006).

For other essays in this series, see http://

nature.com/nature/focus/arts/connections/

index.html

Biologys next revolutionThe emerging picture of microbes as gene-swapping collectives demands a revision of such

concepts as organism, species and evolution itself.

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Putting the pieces together

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