desert green algae in these biological crusts and their close evolutionary connections with freshwater algal ancestors.4 Occasionally mosses can be found amongst
these crusts, rubbing along perfectly well with the fungi, cyanobacteria, and algae.
Sand-locked desert mosses charmingly exploit the morning dew that collects
on their shoots for reproduction: it provides the liquid medium for their male
sperm to wriggle through and fertilize the female egg cells to renew the life cycle.
Cyanobacteria, green algae, mosses, and the Joshua trees are related to each other, as Charles Darwin (1809–1882) and Alfred Russel Wallace (1823–1913) brilliantly
realized over a century ago. Darwin adopted a tree as an inspired metaphor for
conveying the essential point that the great variety of life can be traced back to a single common ancestor, with all branches leading back to a unified trunk. This
became the evolutionary tree of life.
The concept of relatedness among all life forms on Earth, past and present, is so familiar to us today that it is easy to forget this has not always been the case. At the close of the seventeenth century, botanists lacked a coherent framework for classifying the diversity of plant life. Sir Isaac Newton (1643–1727) may have begun
writing mathematical equations distilling the fundamental physics of the Universe into his grand Principia Mathematica around this time, but botanists were still struggling to make sense of the world of plants. The English naturalist John Ray
(1627–1703) rode to the rescue when he made the important conceptual break-
through of classifying plants based on similarities and differences in the physical appearance (morphology) of species. The forgotten man of plant taxonomy,
Ray was a contemporary of Newton and rose from being the son of a blacksmith
to become a Fellow of Trinity College, Cambridge. His 1686 Historia Plantarum
16 a FiFt y shades oF green
established, amongst other things, the modern concept of a species, but it fell to the Swedish botanist and physician Carolus Linnaeus (Carl von Linné; 1707–1778)
to establish the science of classification—the systematic ordering of nature.
Collecting and studying plants was Linnaeus’s first love. He occasionally hit the buffers with his (for the time) controversial principles for classifying flowering plants based on their male and female reproductive parts. His genius found
expression, however, when it came to the describing, naming, and grouping of
organisms, establishing the principles for classifying them into a hierarchy of
relationships. Not a man noted for his modesty, his favourite aphorism was ‘God
creates and Linnaeus classifies’. He also wrote four autobiographical memoirs, published after his death, to ensure his achievements would outlive him.5 A charming and popular teacher, Linnaeus was admired and respected by his contemporaries
and students alike.
Darwin and Wallace, modest men by comparison, explained how the diversity
of life obsessively catalogued by the Swede came about. Their celebrated theory
of evolution by natural selection revolutionized biologists’ world view as much
as Newton’s Principia had revolutionized physics and astronomy nearly two centuries earlier. At a stroke, they breathed evolutionary life into the dry classification of organisms undertaken by Linnaeus as he organized our knowledge of
the living world. Wallace and Darwin gave biology the foundations of a grand
unified theory.
Taking their cue from the concepts of relatedness expressed in the tree of life, the task for taxonomists is to assemble a grand picture of the evolutionary relationships that link together all species of the plant kingdom.6 The tree of plant life currently depicts the patterns of relationships for the three major lineages of plants: glaucophytes (freshwater algae), rhodophytes (red algae), and the Viridiplantae
(chlorophytes, charophytes, and land plants).7 Glaucophytes (also known as glau-
cocystophytes) are obscure microscopic freshwater algae and not an important
group to our story. Red algae and green algae, on the other hand, are both species-rich, diverse groups dwelling successfully in a wide range of environments. Red
algae did not give rise to land plants, but nonetheless deserve a mention, not least because the oldest accepted plant fossils, dated to 1.2 billion years ago, are the remains of red algae. Preserved in rocks of the Canadian high Arctic, these early photosynthesizers are called Bangiomorpha pubescens, because their whiskery filaments, around 2 mm long, closely resemble the bristling living red alga Bangia.
FiFty shades oF green a 17
They grew attached to shoreline rocks with holdfast structures.8 Red algae get their colour from specialized light-harvesting complexes of pigmented proteins
called phycobilisomes. The proteins are organized into elegant geometrical
arrangements for efficiently capturing those wavelengths of light not filtered out by seawater, providing a crucial source of solar energy for photosynthesis. Similar pigments are used by the glaucophytes and cyanobacteria.
At the base of the tree there sits a mysterious alga that originated in the primeval oceans around two billion years ago, in the far-off days of the Palaeoproterozoic.9
Destined to shape the future of the planet, and to secure the centrality of plants to life on Earth, it flitted through the ancient oceans powered by a whip-like structure called a flagellum. And it had turned green by acquiring, in an extraordinary way, a chloroplast for conducting the business of photosynthesis.
Chloroplasts are microscopic bodies that are crowded into plant cells. They
contain chlorophyll, the pigment that intercepts sunlight and gives them their
green colour. The acquisition of chloroplasts marks the origin of plants’ ability to photosynthesize; a time when harvests of solar energy and carbon dioxide started
fuelling the biosphere, first in the oceans and then on land. Lynn Margulis (1938–
2011), an influential and flamboyant character from the world of cell biology, calls this a tale of hostage-taking, slavery, and domestication. It all started in the oceans, when a host cell engulfed a free-living photosynthetic cyanobacterium for food.10
Instead of being digested, the cyanobacterium survived and took up permanent
residence; its fate was to become a chloroplast. Chloroplasts, it turns out, are
really photosynthetic bacteria trapped inside plant cells (Figure 1). Millions are packed into leaves and stems, each one a miniature photosynthetic factory, or if
you prefer, an energy transducer, using its chlorophyll pigments to trap solar
energy and convert it into chemical energy for synthesizing organic molecules
from carbon dioxide and water. By an astonishing trick of nature yet to be fully
understood, chloroplasts are persuaded to hand over the sugars they manufacture
by photosynthesis to fuel the host cell’s metabolic activities. Why the complex
union between an alga and a cyanobacterium took place remains a mystery.
We might speculate, as others have, that some change in local environmental
conditions, coupled with a scarcity of prey, made it beneficial to stop eating and start photosynthesizing. Regardless of the why, these benevolent bodies also
conveniently replicate themselves before a plant cell undergoes the upheaval of
dividing into two daughter cells, ensuring that each cell inherits the ability to
18 a FiFt y shades oF green
LIVING TOGETHER—THE THEORY OF
ENDOSYMBIOSIS
-
The acquisitions and mergers of the cellular world, explaining the origin of
the chloroplast and mitochondrion organelles, are part of a phenomenon
called endosymbiosis; meaning literally ‘living together i
nside’. The theory of
endosymbiosis championed by Margulis is widely accepted by the broader
scientific community and was originally proposed at the dawn of the last
century by the Russian biologist Konstantin Mereschkowski (1855–1921).11 As
is often the case when a radical new theory appears, fierce scepticism greeted
the arguments, no matter how carefully laid out before colleagues. Had he
lived, Mereschkowski would have had the last laugh because his endosymbi-
osis theory is now part of mainstream biology, having found an advocate in
Lynn Margulis.
In her lifetime, Margulis saw the discovery of thousands of genes inherited
from the engulfed photosynthetic cyanobacterium in the genomes of green
plants. It is worth quoting here from her obituary written by James Lake, of
the University of California, Los Angeles, in the leading scientific journal
Nature.12 Lake wrote of the moment when Margulis’s paradigm-changing
view first received serious support: ‘As Boston University’s Douglas Zook,
then an undergraduate in one of her classes, recalled, it was an emotional
moment in 1978 when her ideas on endosymbiosis were confirmed. She
strode into class beaming, holding Robert Schwartz and Margaret Dayhoff’s
classic paper, “Origins of prokaryotes, eukaryotes, mitochondria, and
chloroplasts”,13 hot off the press. That paper concluded: “The chloroplasts
share a recent ancestry with the blue-green algae [cyanobacteria]”, and that
“the mitochondrion shares a recent ancestry with certain respiring and
photosynthetic bacteria, the Rhodospirillaceae”. Margulis’s proposals for
endosymbiotic chloroplast and mitochondrial origins had both been proven
in the same paper.’ Based on this account, it is fair to say that 1978 marks a
suitable date for the entry of the theory of endosymbiosis into mainstream
science.
FiFty shades oF green a 19
Ancient
alga
Mitochondrion
Nucleus
Photosynthetic
Chloroplast
alga
Figure 1 Hostage taking and slavery in the ancient oceans. An ancient alga acquired organelles for photosynthesis (chloroplast) and for generating energy by burning oxygen (mitochondrion).
photosynthesize with its own population of chloroplasts.14 Green plants have
been using the same basic photosynthetic machinery, packed into chloroplasts,
more or less unchanged for nearly two billion years since they first captured a
once free-living bacterium.15
Even before the last common ancestor to all green plants irreversibly assimi-
lated a cyanobacterium, it had already pulled a similar trick to gain something else it needed: energy. Small structures inside cells called mitochondria are the vital tiny battery packs generating the chemical energy essential to life. They use
elaborate biochemical pathways that burn oxygen and sugars to fuel the cell, a
process known as aerobic respiration. Margulis argued with careful reasoning
that mitochondria are the remnants of ancient parasitic or predatory free-living
bacteria belonging to the primitive order Rhodospirillaceae, part of a group
known as alpha-proteobacteria. This group includes weird iron-precipitating
microbes which form tiny chains of the iron mineral magnetite, and which have a
similar appearance to nanoparticles sitting on the Martian meteorite ALH84001
found in the Allen Hills of Antarctica in 1984.16 Like chloroplasts, mitochondria are fully adapted to life inside cells, where they too replicate autonomously to provide daughter cells with the battery packs they need to generate energy for fuel-
ling their metabolism.
Equipped with its newly acquired chloroplast, the distant algal ancestor of
green plants swam off into the strange oceans to change the world by transform-
ing the seas and continents of the planet.17 That transformation gathered pace
around a billion years ago, when it gave rise to the two great lineages of plants: the Chlorophyta and Streptophyta (Plate 1). Each division is a large taxonomic
20 a FiFt y shades oF green
grouping called a phylum and each followed its own spectacularly different
evolutionary trajectory.18 Chlorophytes are the green algae that diversified as
plankton in the oceans and radiated into coastal and freshwater environments.
They transformed the planet not by greening the land but by colouring the
oceans; they are only distantly related to land plants. Chlorophytes are important, but streptophytes are the special group for our story. This group comprises the
charophyte green algae, the first algae to conquer freshwater habitats, and land
plants. Today’s charophyte algae are not a particularly species-rich group, num-
bering a few thousand species at most. Their current diminished diversity reflects a progressive thinning-out by cataclysmic upheavals throughout Earth’s history,
especially during the mass extinctions at the end of the Permian and Cretaceous
periods.19 Modern charophyte species make up for this fact by encompassing a
marvellous array of unicellular, filamentous, and complex multicellular forms
that live in shallow or transient freshwater pools and streams, with a few able to survive in terrestrial habitats; damp soils are a favourite. It could even be that the charophycean green algae ancestor possessed a physiology allowing it to cope
with the harsh terrestrial environment and had already been living on land for
some time before the emergence of land plants.20
The close evolutionary relationship between charophyte green algae and land
plants reveals something of singular importance: freshwater algae made the move
from water to land and in doing so laid the foundations for modern plant diver-
sity. It follows that freshwater is the ancestral habitat of the common ancestor of land plants. Plant life did not, as some popular accounts suggest, establish itself on land by ‘storming the beaches’. Instead, this great event in biology began less dramatically, by the stealthy creeping of freshwater algal progenitors of land plants outwards through the soggy sediments of streams, rivers, lakes, and ponds. At
first glance, quieter coastal environments might appear obvious places to make
land. But success here would have demanded highly specialized floras, such as
mangroves or saltmarsh plants.21 Freshwater environments are altogether kinder
to life, as we shall discover. Indeed, it is entirely possible that all fundamental diversification of plant life originated in freshwater, because red algae and the glaucocystophytes may also have evolved there, despite their current importance
in marine environments.22
Botanists are, surprisingly, completely at a loss to explain what caused the
deep evolutionary split within the green lineage creating the chlorophytes and
FiFty shades oF green a 21
the charophytes. Few have been brave enough to venture explanations for the
schism but one hypothesis suggests the onset of ‘Snowball Earth’ conditions as a
possible trigger.23 Burkhard Becker of the University of Cologne is the leading
exponent of this theory, and he points out that the two great lineages of green
algae appeared during a series of major glaciations. Not for nothing is this interval of geological time called the Cryogenian. Geologists continue to debate whether
the Earth could have frozen over completely to entomb the whole planet in ice
each time, with life surviving under o
r above the great ice sheets, or whether
habitable oceans existed in equatorial regions. Becker argues that the intense glaciations of the Cryogenian acted as environmental filters, selecting the best-
adapted green algae from an ancestral pool of photosynthesizers living in
different habitats at the time.24 During the final glaciation of the Cryogenian,
580 million years ago, the major ice sheets once again expanded across the world, slowing the precipitation cycle. Freshwater pools and lakes dried up, forcing the evolutionary hand of algae: adapt to the challenges of a terrestrial existence and survive, or face extinction.
But why did charophyte and not chlorophyte algae give rise to land plants after
the two lineages had diverged from one another a billion years ago? Both cer-
tainly had ample time, hundreds of millions of years, for expansion into new ter-
restrial environments. Part of the explanation could come down to simple matters
of priority and ecological elbow room.25 Charophyte algae colonized freshwater
first and made land first. By the time chlorophyte algae had made their move into freshwater, any descendants evolving terrestrial tendencies would have faced
fierce competition from plants already successfully adapted to the challenges of
life on land.
Large red and brown seaweeds (which are large chlorophyte algae) colonized
the shoreline and evolved complex life cycles, but they never really ‘invaded’ the land. Large fronds attached to rocky shores might seem like obvious progenitors
of our land floras. Seventy years ago, this notion proved irresistible for the
Oxford botanist Arthur H. Church (1865–1937). He proposed that algae from the
intertidal zone were the starting point for the frontal ‘assault’ on land, but we now know they were no such thing. So taken was he with the whole idea that he
postulated a hypothetical, and long extinct, green algal group that launched
what he called a ‘sub-aerial transmigration’.26 Now regarded as little more than
a botanical curiosity, Church’s flight of whimsy reminds us of an important
22 a FiFt y shades oF green
lesson: a proper understanding of evolutionary events demands a robust tree of
evolutionary relationships.
Making Eden Page 4
