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

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.

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

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!!