Symbiosis

When this is, that is.
From the arising of this comes the arising of that.
When this isn't, that isn't.
From the cessation of this comes the cessation of that.
—Idappaccayatā
 

by Elio, Tony Summers, Christoph & Roberto
 

Elio's musings…
 

For as long as I can remember, I have been fascinated by the subject of symbiosis. This is one of the grand themes in biology, what Margaret McFall-Ngai has aptly called the elephant in the room, deserving much love and attention. But exactly, what is it that is so fascinating about it? Why does it have such a strong appeal to the human mind (not just mine, I trust)?

Figure 1. The crocodile and the bird. Sou­­rce. This image is a digital reconstruction of a popu­lar myth attributed to Herodotus, 5th Century BC. Frontispiece: Lichen of the family Parmelia­ce­ae, genus Hypotrachyna. Courtesy of ©2018 Ma­ria M. Zambrano

In search of answers, I engaged some non-scientist din­ner companions and showed them the photo of the croc and a bird, a digital reconstruction of the description of this presumed relationship first put down in writing by Herodotus in the 5th century BC. My friends all said that they found the image bewildering, surprising, astonish­ing, which is what made it interesting. One of my friends hastened to say that such a reaction did not apply to all symbioses and that, for instance, he found lichens unex­ci­ting. I could have argued the point, but I would have had to resort to some arcane biology to do it. Better, I could have countered with cogent examples, such as that of the root nodules of legumes, where the plant-produ­ced flavonoids cause the bacteria to make nodulation factors, leading to nodule formation, all for the sake of supplying the plant with usable nitrogen. Or I could have introduced him to the bobtail squid and the magic of how its luminous bacterial symbionts teach it a circadian cycle, and other such gems. Obviously, the repertoire of fascinating symbioses is boundless, timeless, and priceless.

But my friends had more to say. They wondered, how did this symbiosis get started? How did the croc learn to not to eat the bird and instead let it pick its teeth – as seems the logical sequence – or did the bird somehow start the conversation? Furthermore, how did such behavior get imprinted? Is it to be found in the genes of both croc and bird? Did the mama croc teach her kids to behave accordingly and did the mama bird do that too? Notice that each of their questions is relevant to every last symbiosis and that the answers for each case are likely to be beguiling.

And yet, I still don't quite find the answer to my query: why do symbioses have such a strong ap­peal? Not that these considerations aren't exciting and demanding of one's attention. But there seems to be something more general. Is it just that two genomes working together are so much more interesting than the sum of them acting separately? Oui, mais pourquoi? Is there a simple answer? If you feel you have one, even if it's a complicated one, do let me know.
 

Indeed, the following responses soon appeared.

What follows are the first three responses. The first by Tony Summers, one of Elio's dinner companions. Then Christoph and Roberto offer their comments. We hope our STC readers will add some more.
 

by Tony Summers
 

Your question raised by the photo of the crocodile (it may be an alligator, but who cares?) is still with me. Why is the crocodile/bird relationship so surprising, while other forms of symbiosis are yawners?

Figure 2. Bee laden with pollen. Source

I think it is because for many symbionts, each is doing something that seems completely compatible with its expected individual behavior. Insects, intentionally or not, gather pollen. Flowers and other plants produce pollen and in various ways entice insects – and non-in­sect pollinators alike – to visit. This is normal behavior for insects and flowering plants, so nothing there seems shocking. That's what flowers and pollinators do. Algae may live on rocks or trees; same for fungi. So there is no­thing "unnatural" about them living together as lichens. But birds normally avoid carnivorous predators, and car­nivorous predators like crocodiles normally gobble up juicy small animals within their grasp. Birds cleaning the teeth of large reptiles or mammals is so inconsistent with what we think of as the nature of predators and prey that it astounds us.

Sharks and remoras? Clownfish and anemones? More un­expected behaviors, where one species would a priori be expected to devour or sting the other, yet peaceful co­existence prevails.

I guess my bottom line is that I am more surprised by symbioses in situations where I would ex­pect interspecies conflict than in cases where there may be cause for wonder at how a relation­ship developed but there is nothing unexpected about the behavior of either symbiont.

Stop bugging me with questions that make me think. It's too tiring.
 

by Christoph
 

Let me reflect on what (micro)biologists learned about "symbiosis" during the past century. For one, there is no "barrier" whatsoever between the three kingdoms when it comes to establishing symbioses. It's more a sort of "United Nations" but without a dedicated "security council" and "veto rules." Second, multicellular eukaryotic hosts that rely on the collaboration with microbes for making the most of their diets, and most if not all do, have "explored" (evolutionarily) the full range of contiguity with potential partners. "Full range" means everything, from seasonal asso­ci­a­tions as in the Fungia scutaria (reef coral)–Symbiodinium (dinoflagellate) symbiosis, to long-term associations as among leaf-cutter ants and "their" Lepiotaceae fungi, probably established in the early Tertiary, that is, some 55 – 60 million years ago. The beewolf–S. philanthi (Actinomycetes) symbiosis most likely survived even the last major extinction event. "Full range" also means that hosts and symbionts may remain permanently "outside" each other (ectosymbiosis) as in the sym­biosis of the ciliate Kentrophoros with a thiotrophic Gammaproteobacterium. Alternatively, hosts may house symbionts in specialized organs, as do the ruminants in their forgut compartments, or the thistle tortoise beetle, C. rubiginosa, with its Stammera symbiont. One step closer to organel­les, endosymbionts may be housed within specialized cells. Think of the bacteriocytes of aphids that harbor their Buchnera endosymbionts.

Tired of all the symbioses popping up here in STC on a fairly regular basis? Not me, obviously, but let me tell you why. To some degree, sure, because every newly uncovered symbiosis adds even more flavor to Charles Darwin's poetic claim in the famous 'tangled banks' citation that "...endless forms most beautiful and most wonderful have been, and are being, evolved" (Origin of Species, 1859, p490). But for the major part because every new symbiosis emphasizes that Life on Earth is a "community enterprise" despite the constant struggle for "survival of the fittest."

Figure 3. Dental Plaque as visualized by "CLAS-FISH" technique. Source

Life is, indeed, a community enterprise with the full range of evolutionary possible com­munications, competitions and collaborations across all domains of life. Life is a com­munity enterprise on a planetary scale with respect to the carbon cycle, for example, but also at any imagin­able micro-scale, say, your dental plaque. In fact, a soli­tary lifestyle is probably an exception for an organism, not the rule, and the solitary bacterium Desulforudis au­daxviator is, in this sense, an "extremophile."

Here's a whiff of science history as my final remark. The use of the term "symbiosis" in biology did not start in the 1950s with US-American evolutionary biologist Lynn Mar­gulis (1938–2011) and the theory of "symbiogenesis" she promoted, nor around 1910 with the Russian botanist Konstantin Mereschkowski (1855–1921), but actually da­tes back to the late 19th century. I translate here two sentences from a 1879 paper 'Die Erschein­ung Der Symbiose' by the German mycologist Heinrich Anton de Bary (1831–1888):

...there are many phenomena that join parasitism, mutualism, etc. regarding the asso­ci­a­tion of [phylogenetically] different organisms for a shared existence, but are far more diverse than that they could simply be accommodated in the usual differentiated categories. Parasitism, mutualism, lichenism etc. are each special cases of that general association for which the expression "symbiosis" may serve as collective designation.

Note the unfamiliar term "lichenism," with which the author characterizes the specific association of algae and fungi in lichens, and whose study – already quite advanced in the 1870s – was pro­bab­ly instrumental in developing the concept of symbiosis.
 

by Roberto
 

Figure 4. Yellow billed Oxpeckers perched atop a zebra. Source

I believe Elio's question goes to the heart of what it means to be human and I feel Christoph's answer beau­ti­fully describes the pourquoi of our fascination with sym­bioses. Our minds want answers to the mystery of ex­ist­ence and whenever we see life express intimate asso­ci­a­tions across species we see what Christoph calls the community enterprise, which I like to call the unity of life. But, why were Elio's dinner companions so surprised with the croc and the bird and found a lichen a yawner? I say perspective and lack of full understanding. For one, I am very skeptical of the croc and the bird story; there is scant evidence for it. In fact, the croc and bird image may be surprising because it is incredible or, more precisely, it is not credible because it is not real. It is, as Elio says above, a digital reconstruction of a 2500 year old description. There are, however, many well-documented cases of such cleaning symbioses. Among those, I am particularly taken by the yellow billed ox­pecker (Buphagus africanus), known to eat the ticks off large mammals such as impala, zebra and African buffalo.

I want to thank Christoph for that whiff of history on the concept of symbiosis from the days of Anton de Bary. I'll elaborate further on three specific points regarding symbioses.

First, all of the above examples of symbioses mention bipartite associations that appear mutua­lis­tic. That points to our natural inclination to reduce complexity and favor interactions that benefit both spe­cies involved, perhaps reflecting a hidden idealism in the face of all the conflicts that sur­round us. But I urge us all to pay attention to Anton de Bary's original intent. In his view, symbios­es spanned the entire range from mutualism to parasitism. The meaning of the word is simply "living together," whether cooperating or in conflict. And that's important because most symbioses are indeed dynamic, often shifting from mutualism to parasitism and back. Take the example of the yellow billed oxpecker and the large mammals it perches on. Yes, the bird cleans away the blood-engorged ticks, helping the large animals. But the bird's food is blood and it also pecks at the animal's wounds to keep them open, not so nice. Symbios­es are not all black and white but rather shades of gray.

Second, there is usually much more to an intimate association than meets the eye, which brings me back to the croc and the bird. Let me, for the sake of argument, assume for a moment that the relationship is real. The image in the first figure is simply an instant that does not necessarily tell all about the ecology and evolution of the association. Is it really mutualism? Are there other species involved? The simple view: the croc gets cleaner teeth and the bird gets a meal. But there could be so much more. The bird may sometimes peck a little deeper and bite off bits of the croc's gums. This will get the bird a better meal but will also inflict damage on the croc before it literally snaps back (again, the mutualism shifting to parasitism). In addition, the croc may sometimes be using the bird as bait. The tiny feathered creature is barely a morsel for the huge amphibian and it would probably fly away quickly if the croc attempts to snap his jaw. But the bird might attract an unsuspecting feline and then as the feline pounces on the bird… a real meal will be had by the croc. This last point, largely unlikely in an already unlikely relationship, brings forth the fact that most of the time we reduce symbioses to two interacting partners – note Elio's phrase above: "…two genomes working together…" Yet, when we analyze symbioses more carefully in their broader ecological context, we discover that most of them are way beyond bipartite, involving many more species. Take the example of the leaf-cutting ants that Christoph mentions. Yes, there are the ants and their fungus. But that symbiosis also includes a fungal pathogen and a fungizide-producing bacterium, Pseudonocardia, that the ants carry, and the nitrogen-fixing bacteria in the fungal garden. With time, probably more species will be shown to play a part in that drama. All co-existing and likely all co-evolving. From that perspective, any and all ecosystems are sym­bios­es. Going all the way up to one symbiosis we call Earth.

Figure 5. Cross section of a lichen, blue cells are fungi and red cells are algae (Source: ©2018 Scott Chimileski and Roberto Kolter)

Lastly, I cannot resist going deeper into the lichens be­cause I think Elio could have enlightened his dinner companions who found lichens unexciting and he could have done so without having to resort to arcane biology. He could have said that, in contrast to the very fleeting (read facultative symbiosis) relationship of the croc and the bird, the fungus and alga (or cyanobacterium) asso­ci­ation can be so intimate that they absolutely depend on each other (read obligate symbiosis). Moreover, he could have described lichens as fungi that discovered agri­cul­ture, subjugating and domesticating photosynthetic mi­crobes for their own benefit to the point that now neither partner can thrive on its own. That is just what us humans have done with maize and wheat and so many other crops. We are very much like lichens and that's nothing to yawn about… Isn't life strange? Yes, and wonderfully so!!