June 2016 Environmental Evolution newsletter

SYMBIOGENETICS
GENESIS
Before she died, Lynn Margulis had written a new edition of her book,
Symbiosis In Cell Evolution. As she often did, Lynn sent copies of her
manuscript to colleagues. Perhaps you received a copy and have read Lynn’s
last words on symbiosis, symbiogenesis and her “environmental evolution”,
defined as the effects of the origin and evolution of life on planet Earth. She
had given this fourth edition a new title coined by her son Dorion Sagan,
Symbiogenetics.
The “genetics” within the title refers to genesis, as in symbiogenesis, the
process of evolving composite organisms via symbioses. Unlike the
ecological context of symbiosis, the context for symbiogenesis is evolutional.
Mereschkovsky coined the term over 100 years ago for “the origin of
organisms by the combination or by the association of two or several beings
which enter into symbiosis.” (Sapp, Carrapiço, Zolotonosov, 2002)
“In cases where new behaviors, structures or taxa, i.e., new tissues, new organs,
new species, new genera, or even new phyla emerge, new relationships at many
different levels [i.e., anatomic, metabolic, genetic] can be identified as the
consequence of symbiosis, then symbiogenesis has been demonstrated.”
(Margulis, 2009)
PARADIGM SHIFT OR TREND
The Royal Society, London
Suzan Mazur writes about the
Royal Society meeting,”New
trends in evolutionary biology:
biological, philosophical and
social science perspectives,”
being planned for November
to discuss the shifting
paradigms in fields including
biology, medicine, physiology,
Earth systems science,
evolution studies and “evolutionary” fields within the social sciences. This
meeting promises to be a milestone in science. Unfortunately, Lynn’s last
words on many of the subjects that will be discussed appear unlikely to be in
print in time to have been read by attendees. Lynn will be silent. How unlike
her.
AHEAD OF HER TIME
Lynn Margulis had a mission in writing her fourth edition of Symbiosis In Cell
Evolution and I believe Symbiogenetics would make critical contributions to
the conversation at the Royal Society meeting. Lynn would not let the
assembled gathering ignore context and systems theory. She has much to say
in Symbiogenetics about the need for biology to make sense. Margulis
ignored academic apartheid. She was a multilingual polymath, a gifted
teacher, a thinker who questioned what others accepted and a science
historian who brought the Russian symbiogeneticists contributions to
Anglophone science. She was a taxonomist who based her work on whole
organisms, modes of nutrition and metabolism rather than fragmentary
phylogenies. She was a geneticist who saw the utter absence of context and
system thinking in the gene’s eye view. She recognized that mutations were
rarely beneficial, that bifurcating tree models and natural selection alone were
inadequate to map or explain descent with modification. She was a bona fide
protistologist because these organisms revealed the semes of eukaryosis.
She was a cell biologist who revolutionized the field and has never been
forgiven by lesser “men” for doing so. The list of her wide-ranging interests
goes on: botanist, evolutionist, expert microscopist, biogeochemist,
paleontologist and geoscientist. She was one of NASA’s first PIs and started
its Planetary Biology Internship Program. She collaborated with Lovelock on
Gaia theory, she was a founder of Earth systems science and astrobiology.
Her name is synonymous with symbiosis and SET. She was science’s unruly
Earth mother. Her vision is one of the inspirations for the meeting of the Royal
Society on new trends that seem to demand a paradigm shift.
INCONVENIENT TRUTHS
In Symbiogenetics, Margulis refines her vision of environmental evolution in
the changing geophysical context of Earth since the Hadean eon and provides
a “status report on the unsolved and tricky question of the origin of life
itself.” (Margulis, 2011) She makes her case for the five kingdoms taxonomy
of cellular life. She recognizes Woese and Fox’s discovery of archaebacteria
(Archaea), but she points out the illogic of a domain for eukaryotes which
ignores completely holobionts’ obligate relationships to symbionts and
organelles of symbiotic origin. She reminds us that members of Prokaryotae
(archae-and eu-bacteria) exchange genes and defy classification into
definitions of species.
“Like all evolutionists, we strive to keep taxonomic levels consistent. We
respect and accept work of experts unless they are in frank contradiction
to these principles. We are leery of authors who state evolutionary
conclusions without explicit criteria for taxonomic judgment or whose
internecine disputes preclude any choices. I especially deplore the
ephemeral neologisms of T. Cavalier-Smith. Given the bewildering
diversity of the protoctist kingdom, differing expert opinions worldwide,
and the need of teachers and naturalists to be understood, we are sensitive
to the difficulties inherent in our task: to respect and organize members of
this kingdom.” (Margulis, 2011)
STUCK IN TWO KINGDOMS TAXONOMY
John Archibald’s book One Plus One Equals One, is full of spin,
misdirection and what James A. Shapiro calls “schizophrenia”. Here is an
example, one of Archibald’s adoring descriptions of Thomas CavalierSmith.
!
“Cavalier-Smith's bread and butter is 'protistology'- the study of
everything with a nucleus that isn't an animal, fungus, or plant. If that
strikes you as an odd definition and an ambitious task, you are not alone.
The 'protists' (or protozoans) are a loosely defined grab bag of eukaryotes,
exceptionally diverse in every sense of the word. The vast majority of
protists are single-celled, and it is for this reason that they occupy such a
special place in the hearts and minds of researchers who study the
evolution of eukaryotes. It is from within the protists that the macroscopic
life forms that surround us today sprang. And the protists have been an
invaluable source of clues as to how the very first eukaryotic cell, and its
mitochondrion, must have evolved.
“In the 1980s Cavalier-Smith articulated a provocative hypothesis about
early eukaryotic evolution that fueled research in the field for more than a
decade. It was grounded on his belief that the advent of phagocytosis - 'cell
eating'- was a critical step in the development of the complex cell, one that
researchers tended to ignore. Lynn Margulis, for example. In her original
formulation of eukaryotic cell evolution, Margulis presented both the host cell
and the protomitochondrial endosymbiont as being prokaryotic in nature, but
gave relatively little thought to the problem of how one cell had come to reside
within the other. Other early proponents of endosymbiosis, however, such as
Roger Stanier (1916 -1982) and the Nobelist Christian de Duve (1917- 2013),
felt the issue of phagocytosis was simply too important to be overlooked.”
(Archibald, 2014)
It is odd that ‘protistology’ is referred to within quotes, but that is because we
are back in the archaic Animal-Plant taxonomy of protozoology (the study of
first animals), but they are described using the Five Kingdoms taxonomy as
nucleated organisms that are not “animal, fungus, or plant” [or protophyta, for
that matter]. The second paragraph like many of the references to Lynn
Margulis in Archibald’s book seems carefully crafted to mislead and
disparage. Archibald references only Margulis’s “original formulation of
eukaryotic cell evolution” (presumably from 1967 in her On the Origin of
Mitosing Cells) when claiming that Cavalier-Smith was the first in the 1980s to
articulate the importance of phagocytosis in endosymbiosis. Lynn Margulis it
claims ignored how endosymbionts came to exist inside cells.
“By hypothesis, some of these amoeboids ingested certain motile prokaryotes.
Eventually these, too, became symbiotic in their hosts. The association of the
motile prokaryote with the amoeboid formed primitive amoeboflagellates.” (Sagan [Margulis], 1967)
Margulis was well aware of the
cytoskeleton, the proteinaceous
network of microtubules,
microfilaments and intermediate
filaments in eukaryotes, on which
mitosis, phagocytosis, and a
host of other features such as
cell motility and intracellular
motility depend. Cavalier-Smith
may have been the first neoDarwinist to awaken his thoughtcollective to the role of
phagocytosis in endosymbioses
A long rooted spirochete attachment site on a protist cortex.
in the 1980s, but by that time
TEM: L. Sacchi
Lynn was on her way to describing
how attachment, rather than ingestion of that “motile prokaryote” might better
answer the origin of the cytoskeleton.
ANCIENT ANIMACULES
“The recent focus both on the evolution of cytoskeletal components and on an
autogenous (non-symbiotic) origin of a phagocytosing amitochondriate
eukaryote point to a problem that should be mentioned. That theory, once called
the archezoa hypothesis, now sometimes called the phagocytosing archaeon
theory, envisages that point gradual changes lead to a prokaryotic host that can
perform fully fledged eukaryotic phagocytosis (a quite complex process). These
theories have it that phagocytosis is the key character that enabled the
endosymbiotic origin of mitochondria. A problem common to those
theories is that the phagocytotic, primitively amitochondriate eukaryote
does not need a mitochondrion at all, and if there were some construable
selective advantage then eukaryotes should have arisen from prokaryotes
in multiple lineages independently. [emphasis added] That has always been
one of the weakest aspects of autogenous theories, in addition to the
bioenergetic aspects.” (Martin, Garg and Zimorski, 2015)
EVOLUTION BEFORE ANIMALS
In Symbiogenetics, Margulis looks at the minimal manifestations that must be
considered to define cellular life. She devotes chapters to cell evolution during
the first 3000 million years long overlooked by neo-Darwinists. “When
everything important in evolution happened,” she liked to say. Bacteria
evolved metabolic pathways from sulfidic to aerobic as they changed the
Earth from anoxic to oxic becoming the active components of the selforganized Earth system, Gaia.
She updates her review of the remarkable and long history (Russian and
European) of symbiogenesis, the dynamic evolutionary process of merging,
not the reductio ad absurdum “objective demarcation” adopted by Archibald.
(Cavalier-Smith, 2003). She compares symbiogenesis (merging) to direct
descent (branching) theories of evolution. Lynn notes the “fluctuating fortunes”
of each explanation compared to modern evidence. Lynn Margulis was
keeping score.
“Symbiogenesis, the fundamental source of evolutionary innovation that merges
at least two lineages renders all eukaryotic phylogenetic tree diagrams
erroneous. No ‘tree of life’ exists. Accurate topology represents emergent taxa
as a web or net of life plotted against the international geological time scale.
All ‘tree diagrams’ are intrinsically limited ‘partial phylogenies’ and therefore,
in principle, can not represent this history of life on Earth. Sorry.” (Margulis,
2011)
”[It is] my assertion that we symbiogeneticists have won not only three out of
four but all four out of four in the reconstruction of algal symbiogenesis. The
first three symbioses established were origins of plastids (from cyanobacteria)
the mitochondria from oxygen-respiring bacteria and of the archaebacterial
component of the cytoplasm. The fourth, the main subject of this fourth edition,
is the establishment of the spirochete origin of undulipodia and of the
cytoskeletal microtubule system generally.” (Margulis, 2011)
On her fourth point, her own experts in the new evidence that Margulis
presents in Symbiogenetics do not agree with her that the available evidence
supports her claim of homology as it pertains specifically to spirochetes. The
ubiquitous 9(2)+0 microtubular arrangement in kinetosome-centrioles and the
9(2)+2 pattern of undulipodia form an unmistakeable seme in eukaryotes. But
what were the eubacterial or other symbionts or small replicons that merged
with crenarchaea to form the first eukaryote with a karyomastigont and
cytoskeleton? We may never know or know only approximately because
reconstruction of the past using extant organisms as proxies for ancestral
forms has severe limitations. 3500 million years--or even 1200 million years-is a very long time and the vast majority of organisms that have ever lived on
Earth are extinct and most of those have left no recognizable trace behind.
Lynn Margulis left Symbiogenetics behind five years ago and perhaps only
one person at the Royal Society meeting will have had the opportunity to read
it.
REFERENCES
Archibald, John (2014) One Plus One Equals One: Symbiosis and the evolution of complex
life. Oxford University Press. Oxford, UK
Cavalier-Smith,Thomas (2003) Microbial Muddles, BioScience, 53 (10): 1008-1013
Margulis, Lynn (2009) Symbiogenesis. A New Principle of Evolution - Rediscovery of Boris
Mikhaylovich Kozo-Polyansky (1890–1957), at the International conference: “Charles Darwin
and modern biology,” Institute of the History of Science and Technology, Russian Academy
of Sciences, St. Petersburg
Margulis, Lynn (2011) Symbiogenetics (unpublished manuscript) personal communication.
Martin, Garg and Zimorski (2015) Endosymbiotic theories for eukaryote origin. The Royal
Society, London, UK
Sagan, Lynn (1967) On the Origin of Mitosing Cells. J. Theoret. Biol. 14, 225-274
Sapp, Carrapiço, Zolotonosov (2002) Symbiogenesis: The Hidden Face of Constantin
Merezhkowsky. Hist. Phil. Life Sci., 24: 413-440
LETTERS TO THE EDITOR
BASED ON OBSERVATION
One of Lynn Margulis’s ideas was her concern that the epidemic of syphilis, a
spirochetosis in which the initial symptoms were no longer presenting (perhaps due
to the overuse of antibiotics), was a co-factor in Aquired Immune Deficiency
Syndrome (AIDS), a constellation of symptoms. In 2008, Margulis and biogeochemist, Wolfgang Krumbein, organized a small meeting in Berlin to discuss this and
other spirochetoses. Spirochaete Co-evolution in the Proterozoic Eon: Ecology,
symbiosis, and pathogenesis (an excursion into environmental immunology). For
details see the March 2016 Environmental Evolution newsletter. Scott McFarlane,
President of MacTech Imaging, a company that images fluids to observe and detect
spirochetal infections, writes, “Just read the 2008 2009 Spirochete round bodies
paper you and Lynn wrote. Superb. For the 1000's of hours we've microimaged, much of what you wrote comports with our observations today.”
TREES, MROs and SUPERGROUPIES
In one of my infrequent between-newsletter emails, I wrote, “...check out this paper on
the an amitochondriate eukaryote in Current Biology. Lynn Margulis postulated that the
original fusion of bacteria formed a eukaryote without mitochondria, such as the
parabasalids. Of course the neoDarwinists’ rear guard explains that it has lost its
mitochondria, but for now that is another neoDarwinist assertion without evidence to
suggest that it ever had them.”
To which John Archibald responded, “I was not an author on the paper you mention
above, but I feel I must say that your interpretation of it is simply not grounded in modern
science. First, Monocercomonoides is an oxymonad, not a parabasalid, but it is related to
parabasalids, which have mitochondrion-derived organelles (hydrogenosomes). The
evidence that hydrogenosomes are derived from mitochondria is very, very strong,
including iron-sulfur cluster biosynthesis and the hydrogenosome protein import
apparatus (which is demonstrably homologous to that of mitochondria). As you may
know, hydrogenosomes also exist it some ciliates, where a genome still exists. In these
cases, the hydrogenosome genome speaks strongly to a mitochondrion ancestry. And
there is a whole host of organisms now described with genome-containing organelles that
are biochemically intermediate between hydrogenosomes and classical mitochondria. It’s
a continuum.”
“Monocercomonoides—the organism without the mitochondrion in the Curr Biol
paper—is clearly nested within mitochondrion/hydrogenosome-containing organisms, so
there really is no basis for saying that Monocercomonoides or parabasalids as a whole
is / are ancestrally amitochondriate. Or maybe you are saying that the root of all
eukaryotes lies within a tiny, tiny corner of oxymonad evolution?”
“What I describe above is evidence—biochemical, cell biological, genetic,
phylogenetic evidence that has been accumulating for about 15 years now. I know of
nobody currently working in the field of symbiosis / cell evolution who does not think that
hydrogenosomes and mitochondria share common ancestry. If you think everything I list
above is nothing more than a neoDarwinist assertion, then I’d like to hear the evidence to
the contrary. What is the evidence that supports the hypothesis that parabasalids (and
oxymonads) are ancestrally amitochondriate?”
I am very appreciative that John Archibald reads my writing and is willing to engage on
these issues and I am also completely aware of my own ignorance, however, if I can
follow an argument, I am not blind to weaknesses or assertions that make more of
data than is in evidence. I responded, “Keep in mind that I am talking out of my field. I
am an evolution geographer. If you read what I wrote, you will see that I did not say that
Monocercomonoides is a parabasalid. I said that Lynn maintained that certain protists never
had mitochondria, such as parabasalids. [Cavalier-Smith makes a similar argument for
archezoa.] She was familiar with the neo-Darwinian mainstream view and evidence that
you cite, but believed there were alternative explanations [that MROs and mitochondria
share a common ancestry may not be the same as MROs were once mitochondria]. I have
no idea if she was correct or incorrect in her view. I also realize that Monocercomonoides
is nested within tree models of mitochondrion/hydrogenosome-containing organisms, but
are these bifurcating tree models appropriate when true phylogenies are networks rather
than bifucating trees?”
“I may be reading the paper incorrectly and certainly there is a great deal of the
paper that is over my head, but it seems that the authors (not me) are stating that there is a
lack of evidence that this organism has ever had mitochondria including all of the evidence
you mention with the exception of the tree phylogeny [Tree modeling is also a problem
with Super Groups]. If eukaryosis took place early in what was an anaerobic world or
during the rise of oxygen levels in microoxic environments than it would be reasonable to
think that making mitochondria part of the original symbiogenesis might be putting the cart
before the horse. Certainly the selective pressures and genetic change inducing stress
would have been to deal very early with toxic microoxic environments. Lynn thought that
a sulfur syntrophy might have helped scrub the oxygen from the environment thus giving
rise to new behaviors, new tissues, and the continuum of changes in classic symbiogenesis
as it progressed to fusion of organisms and shared genetic functions. Given the advantages
of oxygen respiration in terms of energy production and the direction of change of
environment from anaerobic to oxic, it seems that losing mitochondria to “return" to
anaerobic environments (where many protists are found) would be difficult to explain and
unparsimonious. It would seem much more straightforward for protists in anaerobic or
microoxic environments to represent life that stayed put in those environments because
they remained stable. Would you agree?”
THE UMASS-AMHERST DEVELOPMENTAL BIOLOGY FILMS CHANNEL
Thoru Pederson writes, “You have been such a champion of all this and everyone is so
grateful. Now having a direct link to the films is so helpful. We will all use and
broadcast this extraordinary treasure trove, as yet another radiance of Lynn.”