Note: This was to have been chapter 10 in my sequence of postings. Due to (yet another) major rearrangement of chapters, this is now chapter 14. The next section, titled “The Microbiosphere,” is in progress. So are following chapters, then a few that I’ve already posted (also relocated). The next bit I will post is chapter 25. Also note that this free blog service has some unexpected limitations regarding formatting, font size, et cet. Weird anomalies in spacing or hyphenation are not sloppy errors on my part. One more thing: this is intended to be a scholarly work; I have a reference list with almost 250 sources, all of which are cited in the text with footnotes. I've left that material out of these posts.
Close cooperation of organisms has been central to the epochal advances in the history of life. It relieved the nucleus of the eukaryotic cell of housekeeping functions, which are carried on by organelles. The multicellular organism is a grand symbiosis of specialized cells, each kind expressing a different part of the genetic instructions of the entirety. Social insects are symbionts in fundamentally the same way, as the different castes take on allotted specialities…. No one can say how much of evolution is competition or cooperation; they are inseparable.
Robert Wesson
After returning from his voyage aboard the Beagle, Darwin was obsessed with the wealth of ideas he had accumulated during his long journey. The Galapagos finches, in particular, haunted his thoughts for years. It was the variety of special adaptations to their environment that convinced him: Species are not fixed and eternal! The problem was, Darwin could not envision a mechanism that would cause them to change over time.
In 1838, only a year after he had begun collecting facts in a notebook to support his slowly maturing theory, Darwin chanced on a work that would help change the course of history. Much later, crediting the influence of an English economist on his concept of natural selection, Darwin wrote:
I happened to read for amusement ‘Malthus on Population,’ and being well prepared to appreciate the struggle for existence which everywhere goes on from long-continued observation of the habits of animals and plants, it at once struck me that under these circumstances favourable variations would tend to be preserved and unfavourable ones to be destroyed. The result of this would be the formation of a new species.
When Malthus, a proponent of laissez-faire capitalism, published An Essay on the Principle of Population (1798) it created quite a stir. Though well-received by fellow economists it outraged many. (Late 18th century England was in the midst of a period of widespread optimism regarding the future of British society and culture.) In his treatise Malthus argued that populations whose growth went unchecked by disease or famine or war would grow “geometrically,” quickly outstripping food supplies. So here, Darwin finally hit upon the mechanism that causes species to change and diverge. He was already intimately acquainted with the harsh realities of life in the natural world.
Malthus’ reasoning and gloomy conclusions had a considerable impact on Darwin’s way of thinking and it was this influence that in due course led to a widespread view of life being dominated by competition and conflict. But here is another perspective—one that is seldom considered: Despite all the suffering and misery our often-harsh world dishes out so lavishly, untold numbers of organisms are granted long and uneventful lives. Regardless of whether one credits animals with having any sort of awareness or sensation of experience, those that manage to survive live through sunny days without hunger or fear or pain, enjoying the sheer gratification—call this what you will—that simply comes with the gift of being alive. I find it odd that the notion of something that could be called “primal contentment”—the elementary pleasure of mortal existence—is not granted survival value. (But then, it would first have to be recognized as a “thing.”)
In contrast, the impression of eternal strife in the natural world has become lastingly fixed in the Western mind. The seed was planted when papers by Darwin and Alfred Russel Wallace were simultaneously presented to the venerable Linnaean Society (this was in London, July of 1858) and the British public was introduced to the concept as word of these electrifying ideas spread. [This is neither the time nor place to recount the well-known story but, in brief: the much-younger Wallace stumbled on an almost identical theory of natural selection after Darwin had been carefully polishing his own version for two decades. Darwin was notified by a mutual acquaintance that Wallace was about to publish his own hypothesis and it was agreed that papers prepared by both authors would be read before an august body of scientists.] Darwin’s piece opened with this severe pronouncement: “All nature is at war, one organism with another, or with external nature.” Wallace’s paper contained equally stark imagery, portraying all living things as being engaged in “a struggle for existence, in which the weakest and least perfectly organized must always succumb.”[1] And of course there is the endlessly referenced snippet lifted from Alfred Lord Tennyson’s famous poetic lament, In Memoriam A.H.H., which has firmly planted in our consciousness a mental picture of blood-drenched fangs and talons.
Over time, this prevailing view of nature’s everlasting violence has begun to shift. Field biologists point out that their observations of ecological communities simply do not square with that harsh depiction. In fact, many have come to see the web of life as not so much endless war as a competitive arena where harmonious interaction is common. Paradoxically, while one of the principal themes exhibited by life is individual autonomy, at the same time there is a robust predisposition to intimate interaction that goes well beyond routine competition. The view that cooperative relationships are the rule and not rare exceptions is gaining authority. This sea change is inclusive of the microscopic world, where it is ever more evident that cooperation and communication within and between populations is routine. The perception that microbes in general are often beneficial and ecologically vital (and that only a handful of microbes are harmful) is gradually taking hold in the public’s awareness.
Of course, to describe ecological relationships using emotionally loaded terms like “harmony” and “cooperation” is not to suggest that such interactions are good, or of an accommodating nature. But then, the use of such “soft” language may serve to help compensate for equally fraught terms connoting competition and strife. Microbial ecologist Forest Rohwer, speaking of our normally beneficial gut microbes, expresses in blunt language the true spirit of such relationships: “If you go immunosuppressed for a little bit, they’ll kill you. When you die, they’ll eat you. They don’t care. It’s not a nice relationship. It’s just biology.” It is difficult to escape certain instances of deeply ingrained bias—for instance, the psychological tendency to see predators as fundamentally bad, when in truth predation is merely one essential aspect of resource exploitation.[2]
There are a number of specific types of relationships between organisms. They can be competitive, cooperative, or exploitative. Organisms whose lives are intimately entwined are said to be involved in some type of symbiosis. Symbioses are characterized according to the nature of the involvement. While their classification is not always clear-cut, the broad categories are as follows: mutualism is an association (properly speaking, a collaboration) that is close and beneficial to both parties; commensalism, which is advantageous to one member and neither harmful nor beneficial to the other. Finally, there is parasitism—strictly biased in favor of one member, the parasite, which profits at a cost to the “host” species but seldom kills it. Endoparasites live inside a host species while ectoparasites inhabit their host’s exterior.
Symbioses are to be found within individual cells or forming planet-wide networks. But it is at either end of this vast spectrum that the benefits of symbiosis become more akin to imperatives. As mentioned in chapter 5, endosymbiosisis a mutualistic association where one organism lives inside another. A representative example is that of microbes living in the guts of animals, assisting with the digestion of certain foods.
There are omnipresent and indispensible forms of endosymbiosis taking place on a subcellular level. In deep antiquity, prokaryotes gained the ability to obtain nourishment by bodily enveloping particles of organic matter in the fashion of amoeba. (That is, as opposed to simply absorbing chemical nutrients.) In this way, primitive bacterial organisms joined together with much larger prokaryote “hosts,” forming what turned out to be a mutually favorable partnership. When biologists first began contemplating this arrangement, it was assumed that the smaller organisms were engulfed prey that somehow managed to avoid assimilation. One such lucky survivor was thought likely to be a cyanobacterium that already possessed chloroplast-like organs capable of harnessing sunlight to make carbohydrates. This merger eventually resulted in the modern plastid (of which the chloroplast is one variety). Another such union likely involved an oxygen-metabolizing bacterium whose descendents gradually morphed into the mitochondrion—the organelle often referred to as the cell’s “power station.” In both cases, the new guests took up residence inside their larger prokaryotic hosts. They never left. And these smaller bacteria’s offspring eventually formed mutualistic partnerships with their host’s progeny, trading energy production for food and lodging. At some point, prokaryotes sequestered their genetic material in a membrane-bound nucleus that developed into a “control center.” (The origin of the nucleus remains one of microbiology’s vexing mysteries.) But somehow these fruitful unions eventually gave rise to primordial eukaryotes, whose far greater organizational and energy-manipulating capabilities made multicellular life feasible. These relationships had vast consequences: without them, our planet would be covered with life, yes, but it would consist of multihued microbial mats—not action-packed forests and jungles and grasslands and deserts. And all Earth’s creatures, magnificent still, would be invisible to the naked eye.
With the idea of eternal strife and struggle being firmly entrenched in our gestalt, the initial bond between the two-cooperating-microorganisms-that-became-one is either couched in terms of the smaller being “enslaved” or “captured.” The larger was “invaded,” perhaps by an endoparasite. (From what we now know about how microbes conduct their affairs, and how sophisticated they had already become, it is just as likely that the host was tricked into accepting its guest.) Endosymbiosis is a prime example of life’s propensity to beget successful relationships. Regardless of how this pact originated, it made complex life a viable life-strategy.
As befell the earliest proto-mitochondria, some kind of archaic cyanobacterium found an inviting home inside a larger prokaryote. When it moved in, this primitive but fully functional prokaryote brought its chloroplasts.Today, diverse groups of animals still carry on symbiotic associations with chlorophyll-bearing unicellular algae. These are most commonly found in marine organisms such as sponges, sea anemones, and corals. Certain types of mollusks—clams, for one—and sea cucumbers have come to rely on algal symbionts as well. On land, some varieties of slugs have chloroplasts derived from food plants incorporated into their surface tissues and these make some nutritive contribution to their host. A different sort of arrangement is that of tree-dwelling sloths with algae growing in their fur; while the algae’s role is unknown, it is generally thought to help camouflage the defenseless, slow-moving mammals.[3]
Symbiosis often takes the form of some type of group interaction, which reaches its apex in the social insects where the theme is so central that colonies of bees, ants, and termites are increasingly being thought of as superorganisms. Crucial to the concept of symbiosis on such a level is this precept: Cooperative alliances function in a hierarchical manner subject to various forms of governance. “Governance” is a recognized but hard-to-define controlling influence affecting all living things in multiple ways. (Even the activities of an individual cell require direction from various modes of higher level control and regulation.) Biological governance is akin to the way government functions in human societies. There, a dominant authority administers networks of interacting entities and the leading body helps distribute the fruits of cooperation. All cooperators benefit; the weaker of them are supported and thus can function optimally as opposed to being out-competed. In nature, as exemplified by the social insects, there is no central adminstrative body—the entire colony participates as a collective, its actions indicative of what can be considered a foretaste of mind.
With all life, governance starts with DNA coordinating and directing cellular activities and reproduction. For eukaryotes, this influence largely—though not exclusively—arises in the nucleus.[4] Again: among all mutualistic relationships, endosymbiosis subject to centralized control is perhaps the most far-reaching; in addition to making multicellular life practicable it imparts the versatility and vigor that helps drive evolutionary diversification. Organized cooperation offers tremendous rewards to cooperators so it is no surprise that the approach is employed throughout the natural world. “Survival of the fittest,” it should be remembered, refers not to the strongest and most aggressive, but to those that are biologically fit—those that are most successful at reproducing.
The competence and efficiency of a heirarchical but non-centralized form of governance as demonstrated by social insects is also found near the very base of the biological totem pole. One of the most extraordinary instances is found in the activities of bacterial consortia—a true form of anarchy. The phenomenon has only recently been brought to light but microbes hit upon the advantages of cooperative living untold millions of years ago. Bacteria can be considered social organisms in much the same way humans are. Many live in what are essentially societies—hierarchical, collaborative groupings of single or multiple species. (The latter are seen in nature in the form of biofilms.) Through a mode of chemical communication known as quorum sensing, microbes make group decisions dependent on population size and density in order to reach some end that only benefits large aggregations. They accomplish this by secreting signaling molecules called autoinducers in response to some stimulus. Bacteria have surface receptors that detect the presence of signaling molecules. When an autoinducer binds to its receptor, it orders up the production of more inducers, which are released into the surroundings. After the inducer reaches some specific concentration a threshold is crossed, triggering a positive feedback loop.[5] Within the population, a host of receptors become activated at virtually the same time in a cascade that initiates other changes. At this point the coordinated “behavior” of the colony can elicit one or more useful responses.
Quorum sensing embodies the essence of cooperative communication and is representative of a theme that takes place, in many guises, throughout the biosphere: the transmission of information via wide-ranging networks. (More on this in the following chapter.) It was discovered in the 1990s through a study involving a bioluminescent marine bacterium, Allivibrio fischeri—in its natural state a solitary, non-photosynthetic planktonic organism. Free-floating individuals make no use of their luminescent capacity as it would serve no purpose and thus be a waste of valuable metabolic energy.
Allivibrio shares an astonishing mutualistic symbiosis with a creature known as the Hawaiian bobtail squid. This tiny cephalopod, only an inch and a half in length, has a bioluminescent organ on its underside. It feeds nocturnally near the ocean surface and can adjust the intensity of a light-producing organ’s glow to match whatever illumination is coming from above. This results in the squid casting no shadow as seen from below, rendering it virtually invisible to predators. By way of some as-yet unidentified mechanism, the diminutive creature exerts a pull on Allivibrio, which enter through special pores before attaching themselves to the light organ’s furrowed surface. This process is aided by special ciliated cells that actively draw in and select Allivibrio (while simultaneously fending off potential microbial competitors) and then foster their growth. Once established, the bacteria cause these ciliated cells—their job complete—to die off. The squid provides nourishment and a protective environment to the bacteria, which multiply rapidly. By communicating through quorum sensing, when the number of bacteria inside a squid reaches around 100 million the entire aggregation lights up.[6]
Among the multitude of symbiotic relationships, many are utterly captivating—staple subjects of nature documentaries. Particularly well-known are examples of mutualism such as those of the yucca moth and the fig wasp, whose exclusive relationship with their host plants have evolved together (known as coevolution) to the point that neither could exist without the other. Then there are the bird and fish “cleaners” that remove parasites from other “client” species, classic examples being the red-billed oxpecker and cleaner wrasse. Several varieties of wrasse, members of a sizeable group of small fishes, live in mutualistic symbioses with much bigger, typically predatory fish that visit “cleaning stations” where a lone cleaner wrasse will scavenge dead tissues and scales as well as searching out parasites, often working within the larger fish’s open mouth. Similarly, the oxpecker is a small bird that grooms outsized African mammals, feeding on whatever it can glean: dead skin, earwax, mucus, blood, and ticks.
This relationship, considered a textbook example of mutualism, is actually far more involved than its usual depiction suggests and could perhaps be better held up to illustrate the perils of accepting an oft-repeated adaptive story as gospel. A recent study points out that much of the literature cites old studies and anecdotal reports. The study revealed that, not only do the birds not significantly reduce the number of ticks carried by a group of cattle, the birds repeatedly peck at open wounds to feed on blood, preventing open wounds from healing. Also, while the removal of encrusted earwax might appeal to our sense of modern hygiene, earwax clearly serves some purpose (it might have antibacterial properties, for one thing) and has an energetic cost to produce. Finally, the relationship between oxpeckers and their clients may vary geographically, seasonally, or be beneficial for one client species and harmful or neutral to another.
There are several approaches to mutualistic symbiosis that should be at least mentioned to help set the table for a broader view—that is, an awareness of symbiotic associations as being part of a global-scale biological process involving all life-forms (the subject of the next chapter).
Lichens are fungi living in intimate association with photosynthetic microorganisms—various types of algae or cyanobacteria. This partnership is so intimate that lichens are given binomial scientific names as if they were distinct species. There are around 17,000 varieties. They are found living on rocks, bark, rotting wood, or dangle from twigs and branches. One of nature’s most successful collaborations, lichens have existed on land for at least 420 million years. Lichens represent one of many beneficial symbioses connected with soils—in this case, with soil formation. Aside from carbon compounds provided by the photosynthetic partner, lichens subsist on air- and water-borne organic particles along with minerals gleaned from the surface upon which they dwell. Lichens secrete acids that encourage mineral absorption, at the same time helping break down rock—a crucial first step in soil development.
Plants in the legume, or pea family have ancient association with so-called “nitrogen fixing” bacteria that live in root nodules and convert atmospheric nitrogen (N₂) into compounds readily available for use. (This utterly vital symbiosis will be explored in more detail shortly.) Nitrogenous compounds, essential for plant growth and development, are in short supply in nature. The industrial process employed in manufacturing the very same compounds for use as crop fertilizers was first discovered in 1913 (originally for making explosives) and is very energy-intensive, being carried out under extreme pressure and at high temperatures. Soil-dwelling bacteria, however, have been producing these chemicals for hundreds of millions of years.
Various microscopic fungal organisms live in close association with plant roots as well, providing a number of advantages such as improving water uptake, supplying plants with nitrogen and phosphorus along with other mineral nutrients from the surroundings. Plants, in turn, deliver photosynthetically derived nourishment to their mutualistic partners. It is estimated that 90% of land plants have these mycorrhizae growing on their roots, without which 80% would wither and die. This relationship has been ongoing since the origin of land plants in the Ordovician period, as evidenced by 450 million year old plant fossils displaying swollen root material.[7] In fact, as Lynn Margulis stated, “Fungi and plants were already locked into productive symbioses at the very beginning of their tenure on dry land.”
Then, there are the numerous associations between animals and microbes. Many involve bacteria capable of breaking down tough food products into digestible form.
Many termite species have endosymbiotic protozoa and other microbes living in their abdomens. These organisms possess enzymes capable of breaking down cellulose, the main food source of wood-eating termites. A strange protist (the term for single-celled eukaryotes) known as Mixotricha paradoxa lives in the hindgut of a single species of tropical wood-eating termite found in northern Australia. Mixotricha is itself in a mutualistic relationship with four different bacterial symbionts that live both on and inside the protist. Around a quarter million spirochete bacteria attached to Mixotricha’s surface provide locomotion through the coordinated waving of their cilia. A similar number of rod-shaped bacteria imbedded in the protist’s surface supply the spirochetes with ATP. In addition, much smaller numbers of two types of spherical bacteria inside Mixotricha act in lieu of energy-producing mitochondria (which the protist otherwise lacks or has lost). Altogether, then, this unique organism possesses five different genomes, earning it votes for being “the ‘poster protist’ for symbiogenesis.”
The distinction between an organism and its mutualistic partners is becoming blurred. Increasingly, higher animals are being considered colonial organisms rather than autonomous individuals. Recall that the human body is comprised of somewhat more microbes than tissue cells. The vast majority are found in the gut but they flourish in every nook and cranny: skin, mouth…even throughout our lungs (which, until recently, were thought to be a bacteria-free, sterile environment). Symbiotic bacteria are often the first line of defense in immune systems. They are of particular importance in helping craft and calibrate immune responses early in life. (If all this seems contradictory, take into account that these helpful microbes are defending their hearth and home.)
Commensal relationships also abound. Microscopic Demodex mites reside in glands on the rims of our eyelids and in hair follicles. Recent assays have revealed that, not only are there millions of bacteria, yeast, and fungi on every square inch of our skin, but different species live in highly specific areas depending on moisture availability. Oddly, some species are found on the right hand side of the body but not on the left. But considering what we now know about intimate biological relationships, it is likely that many of these associations confer unknown benefits to the host.
Parasitism is ubiquitous—another universal theme in the living world. Carl Zimmer writes, “Wherever there is life, there are parasites. There are ten billion viruses in every quart of seawater. There are parasitic flatworms that can live in the bladders of desert toads, which stay buried underground for eleven months of the year; there are parasitic crustaceans that live only in the eye of the Greenland shark, which swims in the icy darkness of the Arctic Ocean…. By some estimates, four out of every five species are parasites.”[8] And while parasitism, like predation, inevitably bears negative connotations, just as with predation it leads to a balanced coexistence with benefits—not to only to populations and species but to the individuals afflicted. Many host animals carry multiple kinds of parasites, both internal and external, but show little ill effect. Rather, a host is impaired when parasites are present in excessive numbers (a graphic example being moose or reindeer in northern latitudes during mosquito season; individuals obviously suffer and can actually perish from blood loss). On the other hand, there is growing evidence that parasites confer specific benefits that enhance their host’s vigor and overall health. Recent research suggests that modern health problems in advanced countries may be traced to a lack of internal parasites. Patients suffering from debilitating Crohn’s disease have responded positively to the (re)introduction of intestinal worms—a “rewilding” of the gut through what is called, aptly, “worm therapy.”
Last but not least: one of the central aspects in a global biotic symbiosis is the role played by decomposers and scavengers, those organisms carrying out the crucial task of removing and recycling no-longer-living organic matter. Decomposers (also known as saprobes) include fungi, bacteria, slime molds, worms, snails, and many kinds of arthropods such as crayfish, beetles, and sowbugs. They initiate the decay of plant, animal, and fecal material. Of particular importance are wood-decomposing saprophytic fungi that release enzymes capable of breaking down cellulose and lignin (the tough, durable ingredient of woody material), both of which are highly resistant to decay. Fungi produce hyphae—fast-growing, threadlike filaments that both mechanically and chemically break down the decomposing material. Fungi absorb nutrients from decaying woody tissues. Few organisms are capable of digesting lignin; those that can—notably the termites—are able to because of their aforementioned endosymbionts. Decomposers perform a vital service by recirculating immense amounts of carbon and nitrogen. (They form links in other biogeochemical cycles as well.) Of course, marine and freshwater ecosystems have their own complex webs of decomposers.
The breakdown of organic matter does not occur in the absence of decomposers. It is important to recognize that these materials do not simply rot and fall apart on their own; decomposition is not just the outcome of chemical action—it is a biological process. Prokaryotic microbes are the only organisms capable of breaking down inorganic molecules containing essential elements such as phosphorus, sulphur, and iron. By converting organic material to humus (the organic, non-mineral fraction of soils), saprobes play an essential role in soil formation. In forming humus, decomposers improve soil structure and moisture retention, add ions and oxygen, provide nutrients in forms that can be taken up by plant roots, and support entire webs of vital soil-dwelling organisms. When they die, they too are reduced by their kindred. The vital role of saprobes cannot be overstated.
Life has many means at its disposal for preserving or re-establishing equilibrium. There appears to be some sort of overarching harmony pervading the entire biosphere that helps maintain a balanced state. It involves symbioses we may not yet perceive—subtle associations that function in unfamiliar ways or over long time spans. In sum: symbiosis takes many forms and operates at scales from the microscopic to global, figuratively making the living world go ‘round.
©2018 by Tim Forsell draft 23 Apr 2018
[1]Neither of the men were present—Darwin was ill and Wallace was still in Indonesia. The meeting aroused surprisingly little interest at the time and it was not until the publication of Origin the following year that these ideas exploded in the public’s consciousness.
[2]Viewing the cruelty and carnage inherent to nature in a neutral fashion is a mind-set that biologists and ecologists actively cultivate. And there comes a point where one can perceive an underlying “appropriateness,” even beauty, in nature’s violence.
[3]In addition to providing camouflage, recent research indicates that two-toed sloths (the sub-group with a highly restricted diet) consume the algae while grooming—chemical analysis shows that the nitrogen-rich material found in their forestomach has as many carbohydrates but considerably more fat energy than their coarse leafy diet provides.
[4]Mitochondria and chloroplasts have surrendered the bulk of their genetic material to the nucleus, which then largely maintains these organelles even while they retain a degree of autonomy, particularly as regards their own reproduction. Outside the nucleus and independent of its direct influence, numerous kinds of protein sensors and their receptors carry out regulatory functions that affect a multitude of cellular processes.
[5]In a physiological sense, a positive feedback loopinvolves a change in some system triggering mechanisms which augment the effects of that change. Positive feedback forms a “loop” when whatever effect has been amplified “feeds back” into the system, maintaining its influence until a regulating device checks the momentum of the modifying influence.
[6]A. fischeri does not adjust the intensity of its own light output; the squid does so mechanically by adjusting the light organ’s position in relation to a reflective surface or hiding it entirely behind the ink sac.
[7]Well-preserved plant remains found in the famous Rhynie cherts of Scotland contain microscopic spore-like structures, chlamydospores, associated with mycorrhizal fungal threads.
[8]According to Campbell Biology, 11th ed., probably more than a third of all known species are parasites.
