Friday, July 17, 2009

Greening the Earth

It's an interesting question, when did photosynthetic life first invade dry land, and what type was it? The tradition is that green plants first invaded the land in the Ordovician or Silurian, if not later, sometime after 500 MYA,[7] well after the Cambrian, when we first see fossils of animals developing in the ocean (there are actually some from earlier, but those may not be animals, and we know little about them). However, there are various lines of evidence that there was already extensive land-based photosynthesis going on a good deal earlier,[3] [4] including a very recent paper:[2] The late Precambrian greening of the Earth (by L. Paul Knauth and Martin J. Kennedy, unfortunately behind a paywall), which examined the correspondence of ratios of carbon isotopes and oxygen isotopes in precambrian deposits, specifically from areas influenced by runoff from continents:
Here we compile all published oxygen and carbon isotope data for Neoproterozoic marine carbonates, and consider them in terms of processes known to alter the isotopic composition during transformation of the initial precipitate into limestone/dolostone. We show that the combined oxygen and carbon isotope systematics are identical to those of well-understood Phanerozoic examples that lithified in coastal pore fluids, receiving a large groundwater influx of photosynthetic carbon from terrestrial phytomass. Rather than being perturbations to the carbon cycle, widely reported decreases in 13C/12C in Neoproterozoic carbonates are more easily interpreted in the same way as is done for Phanerozoic examples. This influx of terrestrial carbon is not apparent in carbonates older than ~850 Myr, so we infer an explosion of photosynthesizing communities on late Precambrian land surfaces. As a result, biotically enhanced weathering generated carbon-bearing soils on a large scale and their detrital sedimentation sequestered carbon. This facilitated a rise in O2 necessary for the expansion of multicellular life.
This analysis basically plotted the isotope ratios from thousands of observations on a two-dimensional axis, and observed that those from after about 850MYA fell into the same groups whether they were after the beginning of the Cambrian or before. This leads to the very plausible conclusion that photosynthesizers had colonized the land and were producing large amounts of carbon-rich detritus that was then oxidized and deposited.

This has some interesting implications: ...
The contrasting isotope data between 850 Myr ago and the Neoproterozoic suggest that the terrestrial expansion of photosynthesizing communities preceded the significant climate perturbations of the late Precambrian glaciations, and was followed by a rise of O2 ([ref]) and a secular change in terrestrial sediment composition. The onset of significant biotically enhanced terrestrial weathering would have increased the flux of lithophile nutrient elements and clay minerals to continental margins. This would have increased production and burial preservation of organic C towards modern values and consequently facilitated the stepwise rise in atmospheric O2 necessary to support multicellularity. The terrestrial expansion of an extensive, simple land biota indicated by the isotope data may thus have been a critical step in the transition from the Precambrian to the Phanerozoic world.
The biggest problem with this is the lack of fossils identifiable as from plants, although the "squishier" plants leave few fossils.

There is one very important feature of plants that allowed them to colonize the land: the invention of mixtures of lignin and cellulose that protects them against the "soft" ultraviolet radiation (UV) that makes it through the ozone layer. This mixture, in turn, depends on a synthesis pathway that begins with an enzyme called Phenylalanine Ammonia Lyase (PAL), "which catalyses the first and essential step of the general phenylpropanoid pathway, leading from phenylalanine to p-Coumaric acid and p-Coumaroyl-CoA, the entry points of the flavonoids and lignin routes."[8]

Another very recent paper, A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land (by Giovanni Emiliani, Marco Fondi, Renato Fani, and Simonetta Gribaldo) reports an intriguing discovery: that the gene for this enzyme was almost certainly acquired via horizontal gene transfer from a soil bacterium, or perhaps from a fungus that had in turn acquired it from a soil bacterium. What they did was to examine the phylogenetic tree of "160 representative sequences" from various species, discovering that all the genes in plants and fungi are descended from a single ancestor related to those of one bacterial lineage. This gene "is homologous to histidine ammonia lyase (HAL), which is involved in the catabolism of histidine and is widespread in prokaryotes and eukaryotes [refs]. It has been proposed that "PAL developed from HAL when fungi and plants diverged from the other kingdoms" [ref]. However, the current view of eukaryotic evolution based on phylogenetic analyses indicates that fungi and plants do not share an exclusive ancestor [refs]. In fact, Fungi are more related to Animals than to land plants. Moreover, land plants belong to the phylum Plantae, which also includes Glaucocystophytes, red algae, and green algae [refs]."

Figure 1: Phylogenetic tree of HAL/PAL gene. Click on image to see original with caption. (From Ref 8 Figure 2)

This, combined with the observations of Knauth et al., brings us to an interesting suggestion: is it possible that, before green plants invaded the land, it was covered with lichens? Lichens, even today, often grow in areas that are heavily exposed to sunlight (UV) but lack the soil necessary for plant roots (and their symbiotic association with certain fungi). Absent plants, they may well have been able to colonize just about any area with sufficient rainfall to provide the water they needed. Lichens are known to invade rock for nutrients,[6] and even cyanobacteria, one of the groups of algae that for symbiotic relationships with fungi to create lichens can chemically erode rocks.[5] The possibility that there was a coating of lichens over most of the Earth's surface as long as 850MYA is quite intriguing.

An obvious question is: what, if anything, ate these lichens? Here I want to hark back to a suggestion I made a while back, regarding the origin of multi-celled animals, and probably other forms of life:
Could it be that the common ancestor of fungi and animals was actually multinucleate, an amoeba-like creature with lots of nuclei, a flexible shape, and a feeding pattern based on engulfing its food?

Such a creature would be well positioned to evolve into both fungi and metazoans, with the latter branch having lots of collared flagelli. The question is, why evolve multiple cells? The answer could well be an explosive adaptive radiation of invasive, intracellular predators. Such an explosion would explain the sudden acquisition of multicellularity by many lineages.
It isn't just animals and fungi that would be so descended, and it's quite possible that a variety of multinucleate amoeboids were present in these early times that fed on the early lichens I've proposed. (Indeed, there are many such today. These may well have lived in small, shaded tunnels during the day (when solar UV may well have threatened them), and come out at night to feed on the upper levels of the lichens. The lichens themselves may have used some form of lignin (or dyes depending on PAL for synthesis) to protect themselves from the sun, although another possibility is that they shed their upper levels as they were damaged, regrowing from cells located deeper, where they were protected from UV. Or it could have been a combination of both.

The possibility that there was a full-blown ecosystem present on the land this long before the Cambrian offers exciting possibilities in understanding the earliest evolution of the animals (in the ocean), as it would have provided large quantities of detritus for food, along with the oxygen needed to take advantage of it. Especially important is that it this would have been true during the two proposed eras of "snowball earth" or "Slushball Earth", when glaciation extended quite far towards the equator: large areas of the earth's coastline would have experienced freezing temperatures along with intense sunlight.

This is important because water close to the freezing point can actually contain enough oxygen to function as blood in an animal that isn't too active, unlike warmer water. This means that animals during those periods might have invented sophisticated circulatory systems, carrying oxygen for all their needs, without the need for cells containing haemoglobin or some other compound specialized for carrying larger amounts of oxygen. By the time the glacial ages were over, presumably some lineages (at least of chordates) had already developed blood cells containing haemoglobin, thus kicking off the chordate/vertebrate adaptive explosion.

Knauth, L., & Kennedy, M. (2009). The late Precambrian greening of the Earth Nature DOI: 10.1038/nature08213

Emiliani, G., Fondi, M., Fani, R., & Gribaldo, S. (2009). A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land Biology Direct, 4 (1) DOI: 10.1186/1745-6150-4-7

Links: (I've included only those links called out in this leader.)These are almost all behind paywalls, unfortunately. I wish they weren't, but...

1.  Plant-driven fungal weathering: Early stages of mineral alteration at the nanometer scale paywall

2.  The late Precambrian greening of the Earth paywall

3.  Late Precambrian Oxygenation; Inception of the Clay Mineral Factory free registration required

4.  Molecular Evidence for the Early Colonization of Land by Fungi and Plants free registration required

5.  Effect of cyanobacterial growth on biotite surfaces under laboratory nutrient-limited conditions paywall

6.  Mineralogical transformation of bioweathered granitic biotite, studied by HRTEM; evidence for a new pathway in lichen activity paywall

7.  The early development of terrestrial ecosystems

8.  A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land

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