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Aquifexpyrophilus, a marine hyperthermophilic microaerophile, length 2.5 microns, with an optimal growth temperature of 85°C (upper limit 95°C). (Courtesy of K. O. Stetter.)

later in Earth history (Dyer and Obar 1994). Low levels of free oxygen preceding oxygenic photosynthesis may have been generated by photodissociation of water, or by high temperature pyrolysis close to erupting lava. If oxygenic photosynthesis occurred by no later than 3.5 Ga (Schopf 1992) the occurrence of aerobic microenvironments, with pO2 on the order of 1 bar (e.g., in cyanobacterial mats) plausibly predated the emergence of aerobic eucaryotes. Knauth (1998) proposed that prior to about 2 Ga oxygen solubility in the ocean was lower than in later times because of the combined effect of high salinity and high temperature. He suggested that the lack of oxygen may have held up the emergence of metazoans. However, his contention that early oceans were highly saline is contingent on the absence of continental platforms (sites of salt deposition), a debatable assumption (see discussion on continental growth rates in the Appendix to this chapter). Moreover, aerobic conditions in the ocean should still have occurred in regions of high cyano-bacterial productivity prior to 2 Ga. Indeed, the carbon isotopic record of kerogens apparently supports this conclusion (Strauss et al. 1992a). Thus, the lower limits of pO2 in surface microenvironments for the emergence of aerobic eucaryotes and Metazoa may have be reached earlier than their upper temperature limits (60°C and 50°C, respectively). The rise of atmospheric oxygen by 1.9 Ga (15% PAL according to Holland 1994) predated the emergence of Metazoa, which may require less than approximately 2% PAL (e.g., mud-dwelling nematodes; see Runnegar 1991). On the other hand, the rise of atmospheric oxygen may well have constrained the emergence of megascopic eucaryotes, particularly Metazoa, as originally argued by Cloud (1976), with the explanation being the diffusion barrier of larger organisms (Raff 1996).

Thus, why did aerobic environments plausibly sufficient for their metabolism predate the emergence of aerobic eucaryotes and Metazoa by at least 0.5 to 1 billion years? The following possibilities may explain this observation:

1. The earliest aerobic (mitochondrial) eucaryote and Metazoan fossils were not recognized or not preserved.

2. Physical constraints other than oxygen level prevented their emergence; temperature is one likely constraint.

3. Evolution is that slow (probably the least likely explanation, given the rapid evolutionary potential of at least procaryotes as shown in laboratory experiments).

If surface temperature was the critical constraint on microbial evolution as we have suggested (Schwartzman et al. 1993), then the approximate upper temperature limit for viable growth of a microbial group should equal the actual surface temperature at the time of emergence, assuming that an ancient and necessary biochemical character determines the presently determined upper temperature limit of each group. The latter assumption is supported by extensive data base of living thermophilic organisms. No cyano-bacteria have been found to grow above about 70°C, despite an apparent 3.5 billion-year ancestry of oxygenic photosynthesis. Similarly, eucaryotes have an upper limit of 60°C and have had 2 billion years to adapt to life at higher temperatures.

The upper temperature limit for viable growth has been determined for the main organismal groups (table 8-1). This limit is apparently determined by the thermolability of biomolecules (e.g., nucleic acids), organellar mem-

table 8-1.

Upper Temperature Limits for Growth of Living Organisms and Approximate Times of their Emergence

Group

Plants Vascular plants Mosses Metazoa

Aerobic Eucaryotes Procaryotic microbes Cyanobacteria Methanogens Extreme thermophiles

Approximate Upper Temperature Limit (°C)

45 50 50

Time of Emergence (Ga)

Temperatures from Brock and Madigan (1991).

aFossil evidence; for earliest eucaryotes, 2.1 Ga (Han and Runnegar 1992). bPrimitive bryophytes.

Problematic fossil evidence for Metazoa, molecular phylogeny. dMolecular phylogeny.

branes, and enzyme systems (e.g., heat shock proteins) (Brock and Madigan

1991). For example, the mitochondrial membrane is particularly thermo-labile, apparently resulting in an upper temperature limit of 60°C for aerobic eucaryotes. Could the upper temperature limit of 50°C for Metazoa be linked to the thermolability of proteins essential to blastula formation, or of the synthesis of collagen, an essential structural protein? Clearly, fundamental research is needed to better understand the biochemical and biophysical basis for the upper temperature limits of normal metabolism of the organismal groups.

Anaerobic eucaryotes may have preceded aerobic eucaryotes before the endosymbiogenic event creating mitochondria (Sogin et al. 1989), although recent data suggest that the nucleus and mitochondrion arose nearly simultaneously in the eucaryote cell (Sogin 1997; Gray et al. 1999). A higher temperature limit for ancestral amitochondrial than mitochondrial eucaryotes would be consistent with suggestions that mitochondria are more thermola-bile than nuclei. It would be interesting to determine whether any living anaerobic eucaryotes are found to be viable above the apparent limit for aerobic eucaryotes (about 60°C).

We have proposed that surface temperatures were the critical constraint on microbial evolution, determining the timing of major innovation (Schwartzman et al. 1993). Surface temperatures at emergence corresponded to the upper temperature limits for each group (i.e., cyanobacteria 70°C, at 3.5 Ga; aerobic eucaryotes 60°C, at 2.6 Ga; and Metazoa 50°C, at 1.0-1.5 Ga), as shown in figure 8-3 and table 8-1. This temperature history is consistent with inferred climatic paleotemperatures from the oxygen isotopic record of Precambrian cherts and carbonates (see chapter 7).

Fungi now have thermophilic species that can grow to an upper limit of about 62°C (Brock 1978). Because the divergence of fungi and Meta-zoa, sister kingdoms, apparently occurred between 1 and 1.5 Ga (Chapman

1992), it is not clear whether fungi modestly preceded Metazoa, a scenario consistent with fungi's higher upper temperature limit, or that thermophilic fungi adapted more recently to living in a higher temperature environment. Similarly, does the fact that the more deeply rooted bryophytes have a 5°C higher upper temperature limit than do vascular plants indicate an ancient temperature constraint on the order of emergence of these two groups among the Plantae? If the geologic evidence for the occurrence of ice ages is accepted for the late Proterozoic (but see their reinterpretation as possible

Hyporthcrmophiles

Hyporthcrmophiles

Eutarymts

Melaioa

Eutarymts

Melaioa

0

Time B.P. (billion years)

Proposed surface temperature history of Earth, with key evolutionary developments noted. Numbers near curves are the ratios of the present biotic enhancement ofweather-ing to the value at that time (BR) computed for preferred model b.

impacts in Oberbeck et al. 1993 and Rampino 1994) then mean global temperatures reached some 10 to 20°C long before the fossil evidence for Plan-tae. Temperatures of 25 to 43°C near sea level are also indicated from the chert oxygen isotope record (Kenny and Knauth 1992). Thus, the possibility of earlier emergence of Plantae is problematical but deserves closer attention. An interesting possibility is that each major innovation first occurred in cooler environments than found in the ocean. The only such plausible environment cooler than at sea level at the high surface temperatures favored here for the Archean/early Proterozoic appears to be mountain lakes, whose sediments and fossils are unlikely to be preserved in the geologic record.

In the scenario outlined above, the genetic potentiality for rapid evolution is simply realized as soon as (relative to a geologic time scale, of course) external conditions allow its expression. If confirmed, this conclusion would have major implications to evolutionary biology and our understanding of the evolution of the biosphere. This explanation of evolutionary emergence is more deterministic than that given by Maynard Smith and Szathmary (1996):

"To explain a particular event, say the origin of eucaryotes, is to show that, given plausible initial conditions, the event, if not inevitable, was at least reasonably likely."

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