(From ISS Symbiosis News, March,
1998, Vol. 1, Issue 3. pp. 1-3)
by Douglas Zook
Associate Professor of Science
Education and Biology
Boston University
The
emerging discipline of symbiosis requires a new vocabulary and even revised
definitions. Words in scientific research and academia, as well as the everyday
world of the public, carry great weight. Words in and of themselves –
even without the definition readily available to the reader – imply
certain meanings and connotations.
Defining symbiosis has almost
become a kind of life science cliché, an act of verbal and often verbose
masochism. There is a long history of debate over symbiosis definition and
usage, dating back to the late nineteenth century original descriptions of Albert
Bernard Frank and Anton De Bary (Sapp, 1994). Their “living together of
unlike organisms” says little in the ecologically-minded perspectives of
today. Unlike organisms are living together all the time, even intimately, but
are hardly examples of symbiosis. A way to make sense of the problem is to
search for and describe fundamental commonalities among those systems that
specialists consider as significantly symbiotic. From these commonalities,
useful definitions can emerge.
All the major symbioses –
including coral-dinoflagellate, Rhizobum-legume, aphids-mycetocyte bacteria, bioluminescent
bacteria with squid and fish, termite-gut microbes, lichens, ruminants with
rumen microbes, forams-algae, mycorrhizae-plants, Azolla-Anabaena – have three distinct
features:
1. By their associations, each
result in a unique or novel metabolism and structure(s), both of which are not
present prior to the symbiosis. As Angela Douglas (1994) points out in her
excellent (now OP) book, Symbiotic Interactions, “The common denominator of
symbiosis is not mutual benefit but a novel metabolic capability, acquired by
one organism from its partners.”
2. Each are so continuously
intimate from generation to generation that their recognition, infection, and
regulation systems would of necessity have to involve very selective
co-evolution with perhaps some ancient or recurrent genetic exchange.
3. The process involves an
acquisition – whether ancient and/or each generation, i.e., one organism
acquires one or more different organisms, and there is enough of selective
advantage that they are maintained through natural selection.
Therefore, I propose: Symbiosis is
the acquisition and maintenance of one or more organisms by another that
results in novel structures and metabolism. Some symbiotic evolution may
involve partner genetic exchanges. Such a definition moves us mercifully away
from outmoded and ambiguous ideas of mutualism, parasitism and commensualism.
Symbiotic systems are in reality more fluid and less linear than such categorizations
allow. It also pushes the discipline to where the action really is – the
genetic basis of the associations and the fact that nearly all symbiotic
systems with broad and even global significance involve at least one
microorganism. It is far more specific to discern and refer to a newly obtained
metabolite or structure through the process than to be focused on extracellular
vs. intracellular and mutual benefit vs. no benefit. Moreover, nearly all the
symbioses result in a new structure, frequently an organ of some kind:
trophosomes, nodules, arbuscles, thalli, mycetomes, intestine, reef, rumen, and
so on.
Symbiosis even from the traditional
definitions should perhaps imply a new and necessary vocabulary as well. For
example, life systems which we deem as symbiotic have a profound impact on the
maintenance and even the origins of biomes and its ecosystems. Nearly all the
grasslands and tropical forest trees thus far examined show necessary
bi-directional metabolite-based relationships with vesicular-arbuscular
mycorrhizae or arbuscular mycorrhizae. Temperate zone shrubs and trees commonly
have associated ectomycorrhizae and over 200 angiosperms require nitrogen
fixing actinobacteria, usually of the genus Frankia. The second most diverse
mega-ecosystem on the planet, the coral reef, is the direct result of
dinoflagellate individuals encysted within the animal tissue. Critical nutrient
cycle movement, including the flow of nutrients from larger inaccessible pieces
to much smaller accessible compounds is facilitated in many ecosystems by
numerous symbiotic insects, such as the termite. Lichens are prevalent in
nearly all imaginable habitats and may even play a key role in epiphyte
distribution and canopy health in the rainforest. These and hundreds of other
examples begin to confer a new picture of life systems on earth. So as to
emphasize this symbiotic importance, as symbiologists, we need to use a term
such as “symbiomes” when referring to grasslands, savannas, boreal
forests, coral reefs, and so on. The term does not imply that all important
events in a biome are symbiotic, but it does convey that the existence of the
biome is in some significant fashion dependant on symbiosis.
An extension of this thinking
suggests that one need not always refer to “ the biosphere.” Those
of us who recognize the global importance of symbiosis should instead commonly
refer to the “symbiosphere.” This is not merely a semantics trick
or juxtaposition of words for new affect. Again, such a term is natural
outgrowth of known research results. They simply have never been promoted from
this perspective. For example, it is widely acknowledge that the plastids in
the entire plant kingdom with many protists as well evolved through the
acquisition and maintenance of another organism, another genome. This symbiosis
impact is multiplied manifold when the symbiotic origin of mitochondria among
the eukarya domain is considered. In short, the influence of symbiosis on the
biosphere has been and remains so profound that one is justified in referring
to the “symbiosphere.”
Historically, the notion of
uncategorizable creatures like Euglena gracilis and Paramecium bursaria has always been prevalent (Sapp,
1994). Overly simplistic or linear taxonomies have even forced us to recognize
that lichens are somehow a part of the fungus kingdom, even though they are
clearly two distinct kingdoms (and in the case of lichens with both green algal
and cyanobacterial symbionts, three kingdoms!). While it is of course
unnecessary to stage any massive uprooting of current phylogenic schemes and
resultant taxonomy, it is worth considering a useful parallel taxonomic scheme,
“Symbionta.” This taxonomic category would recognize that many
representatives of various kingdoms within the three domain system or any other
system for the matter actually merge to, in effect, function as singular,
interdependent genomes. This parallel kingdom would of course include many of
the same organisms in the other kingdoms, but show them directly associated
with their symbionts within various criteria. These criteria could be from the
proposed definition of symbiosis in that new metabolites and structures serve
as the basis, as well as mechanisms of horizontal gene exchange as this becomes
better researched, and even overlapping point mutation trees based on gene
sequencing data. Most importantly, such a grouping would reflect the growing
recognition that so many species, indeed even whole families of organisms did
not evolve independently – rather that they intimately coevolved and even
originated with and within other genomes.
Many of these notions can be
considered an indirect outgrowth, albeit distant, of the ideas expressed
twenty-five years ago by F.J.R. Taylor (1974) and Lynn Margulis (1976) who
proposed a kind of revision of cell nomenclature to allow for the profound
influence of symbiosis. They implied that the term “cell” as a
genome-containing fundamental unit of life was too general and ambiguous. For
example, most eukarya cells contain more than one genome, frequently
symbiotically derived. Thus, it may be more sensible and revealing to refer to
an animal cell as a “dyad,” in that it contains two separate
genomes or gene remnants – one from Arechean like nucleocytoplasmic
ancestor and one from a purple nonsulfur eubacteria that became the
mitochondrion. Plants would be “triads,” in that besides these two,
they have plastids with genes from a cyanobacteia-like ancestor. Some cells
within the protests would be “quadrads” or “quintads,”
for they involve an additional step in which a eukaryotic photosynthetic
organism assimilates, for example, another eukaryotic, photosynthetic organism.
Taylor (1983) also introduced the term “eucell” for a polygenomic,
multi-compartmental, metabolizing unit.
These proposals are not some notion
to layer a segment of the scientific world with more jargon. Instead, we must
become aware that a discipline is recognized only when its vocabulary, its
denotations and connotations – indeed, it’s defining
“scriptures” -- -- are boldly and justifiably used and even
instituted in the context of that discipline.
Douglas, A.E. 1994. Symbiotic Interactions. Oxford: Oxford U. Press.
Margulis, L. 1976. The genetic and evolutionary
consequences of symbiosis. Exp. Parasit. Rev. 39: 277-349.
Sapp, Jan. 1994. Evolution by Association: A
history of Symbiosis.
Oxford: Oxford U. Press.
Taylor, F.J.R. 1974. Implications and extensions of
the serial endosymbiosis theory for the origin of eukaryotes. Taxon 23: 229-258.
Taylor, F.J.R. 1983. Some eco-evolutionary aspects
of intracellular symbiosis. In: International Review of Cytology, Supplement 14, K. Jeon, ed. 1-28.