Life at Middle Age - Biology & Environments on the mid-Proterozoic Earth

Andy Knoll (Harvard University, Cambridge, Massachusetts, USA)

63rd Annual Bownocker Lecture, Department of Geological Sciences,

Ohio State University, Columbus, Ohio, USA

28 April 2005


Check out Knoll (2003) - Life on a Young Planet.

Looking at the mid-Proterozoic - Earth’s middle age.

The initial rise in pO2 in Early Proterozoic resulted in ice ages.  Another rise in pO2 in the Late Proterozoic resulted in ice ages.

There’s been lots of interest in the Early Proterozoic, when O2 began to accumulate, based on chemical evidence.  There’s also been lots of interest in the Early Proterozoic ice ages.  There’s also been lots of interest in the Late Proterozoic rise in pO2 and the Late Proterozoic multiple global ice ages.

These are benchmarks in the history of life as well.  The rise in pO2 allowed life forms to use O2.

The stretch between the Early Proterozoic and the Late Proterozoic has received less attention (= Earth’s middle age).

Looked at the Roper Group (northern Australia) and the Bil’yakh Group (Siberia).


The Bil’yakh Group is a thick carbonate succession exposed along the Catukan River [sp.?].  It's a ~2000 m succession of platform/shelf carbonates, dated to 1.5 b.y.  It includes silicified peritidal carbonates - includes microbially laminated tidal flat sediments.  Early diagenetic silica has preserved micron-level features, including biological features - microfossils.

Ex: 10 micron diameter Eoentophysalis balls - indistinguishable from living Entophysalis (a cyanobacterium) in the same environments today.

So, an introduction to mid-Proterozoic life is an introduction to cyanobacteria.

Cyanobacteria are heroes of the environmental revolution - they invented photosynthetic pathways & released O2.  Most other photosynthetic organisms use cyanobacteria symbiotically.

Cyanobacteria include simple forms, but they mainly include complex colony forms & have complex cell differentiation.

Middle Proterozoic microfossils can be identified as cyanobacteria.

The polysaccharide extracellular envelope of cyanobacterial cells don’t decay easily - they are likely to fossilize.  So, they are easy to recognize and they are easy to preserve.  But, we want to go on beyond morphologies and inferred lifestyles, to broad environmental settings.

Ex: extensive Entophysalis mats in Abu Dhabi coastal settings.

Looking at Earth’s middle age - from 1 to 2 b.y.  We’re finding the same things elsewhere from 1 to 2 b.y.  Lots of cyanobacteria in northern Siberia rocks.  Found trichomes (= filamentous cyanobacteria) - some are short - had recently germinated from resting cells.  Also get sausage-shaped cells (60-70 microns long) in filaments consisting of smaller cells.  This is like modern nostocalean cyanobacteria.  See Archaeoellipsoides.  So, we’re seeing cell differentiation at this time.

Nostocalean cyanobacteria have 3 types of cells - including akinetes, heterocysts.

A cyanobacterial phylogeny has shown that all cyanobacteria that have differentiated cells are part of one clade.  Traditionally, two groups of cyanobacteria have been recognized - both with cell differentiation.  Recent phylogenies show that both groups are in one clade.

By 1500 m.y., cell differentiating cyanobacteria (= derived cyanobacteria) were present.  So, most of cyanobacterial diversity was present by 1 to 2 b.y.

~2400-2100 m.y. is the date for the appearance of this clade.

Most of the cyanobacterial phylogenetic tree is known from mid-Proterozoic rocks.

Proterozoic cyanobacteria were closely related to modern forms - similar physiology, etc.

So, a relatively modern bacterial biota was present in Earth’s middle age.

There were also widespread stromatolites - including large reefs - built by microbes.  Microbes could build reefs comparable in size to reefs seen today.  Microbial reefs were widespread then in the photic zone.  Can see a change in stromatolite form through time.  See stromatolite similarity in rocks of the same age in different localities.  But, different-aged stromatolites show different forms.  Traditionally, this change was attributed to evolution - changes in mat-building biota, resulting in a crude stromatolite biostratigraphy.  The Russians have noticed this for a long time.  But, instead of evolution, the change in stromatolite form corresponds with changes in seawater chemistry.

At 1-2 b.y., peritidal areas had rapid cementation.  On the timescale of bacterial cell decay, surrounding sediments had already cemented/lithified.  See casts/molds of cyanobacterial cells.  There was nearly instantaneous lithification in peritidal settings.  See little fans of carbonate cement crystals.  This isn’t seen in the Late Proterozoic.  So, stromatolite form change is in concert with environmental change.

But, which is the dominant role?  Biological evolution or physical-chemical factors?


Looked at northern Australia (Northern Territories), near the Gulf of Carpentaria.  There’s an extensive mid-Proterozoic succession - well-preserved sediments.  The mid-Proterozoic basins here have been well drilled - looking at ~pristine samples of the Roper Group in drill cores.  Roper Group here is 1429-1492 m.y. - a series of shallowing-upward sequences - mostly siliciclastics: very organic-rich shales, some siltstones/sandstones.  Probable cyanobacteria have been freed up from these shales.  But also, eucaryotic cells have been retrieved - almost 1500 m.y. old.  These eucaryotic fossil cells are an order of magnitude larger than the cyanobacterial cells we’ve looked at.  The eucaryote cells have processes - variable in number, asymmetrically placed, sometimes branching.  So, these are vegetatively active cells - cytoskeleton present - nucleated organisms.  Some minor diversity in eucaryotic cells is seen in rocks of this age.  Larger cells here have surface ornament not known in any bacterial cells.  So, clearly eucaryotes.  Under the SEM, some of these eucaryotic fossils have walls composed of tessellated blocks (hexagons making a closed pattern - not like dinoflagellate paratabulation).  So, these have cell wall ultrastructure.  FTIR (Fourier Transform Infrared spectroscopy) can give a chemical spectrum of a single cell.  Can get chemical constituents of walls of individual cells.  None can be confidently placed in modern eucaryote groups.


Note the presence of 750 m.y. testate amoebae in the Grand Canyon, >750 m.y. green algae from Spitsbergen, 1200 m.y. red algae, 1100 m.y. lipids from alveolates, >1000 m.y. vaucheriacean algae (golden green algae).

So, seeing divergence of major branches of the eucaryotic tree.

Not until the end of the Precambrian do we see diversification (increase in diversity) in eucaryotes.

So, fairly early origins & limited diversity until the end of the Proterozoic.  Then, the Phanerozoic is a eucaryote world.

Soon et al. (2004) - Molecular Biology & Evolution 21: 809 - a molecular clock study, which ~matches the known fossil record.


Now, looking at redox conditions in Proterozoic oceans.

Before 2.4 b.y., there’s no evidence of appreciable O2 in the surface oceanic waters or the atmosphere.  From 2.4 to 2.3 b.y., get a transition to a world with some surface oceanic and atmospheric O2.

Mid-Proterozoic oceans were distinct from today.

Looked at 1.73 b.y. black shales (Wollogorang Fm.) and 1.64 b.y. black shales (Reward Fm.) - at maximum flooding surfaces.

Looked at degree of pyritization and reactive iron content (FeHR/FeT) (portion of highly-reactive iron in sample compared with total iron content).  Found mid-Proterozoic oceans were like euxinic Black Sea sediments.

Roper Group facies - basinal sediments plot in euxinic field & inner/distal shelf sediments plot in oxic field.

Conclusion: low sulfate, redoxcline at moderate depth in mid-Proterozoic oceans - ~10% of sulfate concentration of today’s oceans.

Looking at low sulfate, limited O2 in surface ocean waters.  Below that, anoxic & sulfidic waters.

Anbar et al. (2004) - looking at Mo isotopic trends in mid-Proterozoic interval.

Fe/Mn nodules/crusts form in oxidizing conditions - are a sink for Mo-98.  Modern seawater has a positive d98Mo/95Mo‰.  Mid-Proterozoic oceans had a d98Mo/95Mo‰ value closer to a basalt/granite MoS2 value - consistent with a euxinic ocean then - a not well ventilated ocean then.  This is an independent source of info., with the same conclusion.


Anbar & Knoll (2002) - a speculative paper.

Archean ocean - not oxygenated; high Fe

1250-1850 m.y. old ocean - sulfidic water below surface water having some O2; Mo scarce

Phanerozoic ocean - well oxidized; Fe low


Mo is the most abundant trace element in oceans today.

In mid-Proterozoic oceans, fixed nitrogen not common.  The ability of biotas to fix nitrogen may have been limited by availability of Mo/Fe.

So, expect procaryotes to be the dominant primary producers in mid-Proterozoic oceans.  Expect algae to be most common along the coast, where nitrate & Mo are likely to occur in greatest abundance.

These expectations are met by the mid-Proterozoic record, so far.


Mid-Proterozoic biomarkers recovered:

- 2a-methylopanes and b-carotanes and g-carotanes - from cyanobacteria.

- 3b-methylopane - from methane eating proteobacteria.

- very low steranes - from algae

- chlorobactane and isorenieratane - from green sulfur photobacteria (anaerobic bacteria)

- okenane - from purple sulfur photobacteria (anaerobic bacteria)


So, mid-Proterozoic oceans had O2 in a surface layer and H2S below that (sulfidic).

We’ve been learning much about the mid-Proterozoic - cyanobacteria were abundant, diverse, widespread, modern in diversity & biological function.

Modern cyanobacterial environmental distributions can be used to predict mid-Proterozoic cyanobacterial fossil distributions.

Eucaryote body/cell plans were starting to emerge, but they were not widespread or diverse at this time.

Large diversification in algae/animals only occurred in the Phanerozoic.

“The present is the key to the past” - a statement about processes, not the state of things.  The microbial world today has roots in a world very different from today.  Keep this in mind when looking at microbes in today’s communities.

Before 2.5 b.y., very little O2.

From 2.5 b.y. to ~600 m.y. - some O2.

Since the beginning of the Phanerozoic - lots of O2.



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