The conflict beneath your feet: tradeoffs between attracting beneficial microbes and repelling parasites in the plant root microbiome

A guest author blog by Dr Cor­lett Wolfe Wood

Nearly all organ­isms rely on oth­er spe­cies to per­form cru­cial physiolo­gic­al func­tions, from digest­ing food to fight­ing dis­ease. Bene­fi­cial microbes in our own gut, for example, are an essen­tial com­pon­ent of digest­ive health. Such cooper­at­ive inter­ac­tions between spe­cies, known as mutu­al­isms, are evol­u­tion­ar­ily ancient and are key­stone com­pon­ents of many ecosystems.

But what if it’s dif­fi­cult to tell friends and enemies apart?

Dis­tin­guish­ing mutu­al­ists from harm­ful para­sites is often easi­er said than done. Many spe­cies are attacked by para­sites and patho­gens that are remark­ably sim­il­ar to their mutu­al­ists. In fact, cir­cum­stan­tial evid­ence raises the intriguing pos­sib­il­ity that para­site infec­tion is an unavoid­able cost of form­ing mutu­al­isms. Some spe­cies have co-opted genes used to defend against para­sites to reg­u­late inter­ac­tions with their mutu­al­ists. Oth­ers sup­press immune func­tion when attract­ing mutu­al­ists, leav­ing them­selves vul­ner­able to infection.

Para­sites’ resemb­lance of mutu­al­ists poses a major para­dox: how do organ­isms attract bene­fi­cial part­ners while repelling para­sites? We hypo­thes­ized that the shared genet­ic con­trol of mutu­al­ism and para­sit­ism is likely to cre­ate a tradeoff between attract­ing mutu­al­ists and repelling para­sites, a phe­nomen­on known as genet­ic con­flict.

The con­flict beneath your feet

Although there are com­pel­ling reas­ons to expect that attract­ing mutu­al­ists trades off with res­ist­ing para­sites, dir­ect evid­ence is sur­pris­ingly scarce.  One reas­on is that mutu­al­ists and para­sites often live deep inside the host’s tis­sues (in the digest­ive sys­tem, for example), mak­ing them dif­fi­cult to observe. To get around this prob­lem, we stud­ied microbes that live on plant roots in spe­cial­ized struc­tures that are vis­ible to the naked eye.

Plant roots are a lot like anim­al guts: both are respons­ible for nutri­ent uptake, and both rely heav­ily on microbes for help. Legumes—plants like peas and beans, as well as clovers and alfalfa—take the remark­able step of build­ing spe­cial­ized organs to house their root-asso­ci­ated microbes. If you dig up a bean plant in your garden or a clover in your yard, you’ll find that the roots are covered with small lumps known as nod­ules (Fig­ure 1, top). Inside these nod­ules are colon­ies of mutu­al­ist­ic nitro­gen-fix­ing bac­teria. These bac­teria provide their legume host with nitrogen—a cru­cial nutri­ent for plant growth—in exchange for shel­ter and carbohydrates.

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Fig­ure 1. The struc­tures that mutu­al­ist­ic bac­teria and para­sit­ic nem­at­odes form on legume roots. Photo cred­it: Cor­lett Wolfe Wood.

Unfor­tu­nately for legumes, mutu­al­ist­ic bac­teria aren’t the only microbes that col­on­ize roots. For nearly a cen­tury, farm­ers, bot­an­ists, and garden­ers have recog­nized that some nod­ule-like struc­tures are actu­ally galls formed by para­sit­ic worms called nem­at­odes (Fig­ure 1, bot­tom). Unlike mutu­al­ist­ic bac­teria, para­sit­ic nem­at­odes harm their host. They steal nutri­ents from the plant without provid­ing any bene­fit in return.

Nem­at­ode galls look so much like bac­teri­al nod­ules that the Mis­souri Botan­ic­al Garden warns home garden­ers to take care not to con­fuse the two struc­tures. Moreover, past research showed that some of the same plant genes are involved in build­ing both struc­tures. Giv­en the strik­ing sim­il­ar­it­ies between nod­ules and galls, we wondered wheth­er legumes could form one without form­ing the oth­er.  Can legumes build nod­ules for mutu­al­ist­ic bac­teria without becom­ing infec­ted by para­sit­ic nematodes?

Clovers that aren’t so lucky

We tested our hypo­thes­is using a small weedy plant called a medick (Medica­go trun­catula), a close rel­at­ive of clovers and alfalfa. We grew hun­dreds of these plants in the rooftop green­houses at the Uni­ver­sity of Toronto, and inocu­lated them with mutu­al­ist­ic bac­teria and para­sit­ic nem­at­odes. Just as we pre­dicted, medicks that were good mutu­al­ists were more sus­cept­ible to nem­at­ode infec­tion (Fig­ure 2). Plants that formed many bac­teri­al nod­ules also formed huge num­bers of nem­at­ode galls, while those with few nod­ules formed only a hand­ful of galls. Sib­lings formed sim­il­ar num­bers of nod­ules and galls, sug­gest­ing the two struc­tures share the same genet­ic basis.

To our sur­prise, one medick fam­ily escaped the tradeoff between attract­ing bac­teria and repelling nem­at­odes. These plants formed hun­dreds of nod­ules but hardly any galls at all (Fig­ure 2, bot­tom right corner). This fam­ily is remark­able because it sug­gests that although genet­ic con­flict between mutu­al­ism and para­sit­ism may be com­mon, it is not ines­cap­able: evol­u­tion can find a way out.

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Fig­ure 2. Medick fam­il­ies that formed more bac­teria nod­ules also formed more nem­at­ode galls, demon­strat­ing that the best mutu­al­ists were also the most sus­cept­ible to para­site infec­tion. Mod­i­fied from Wood et al. 2018.

What’s next?

My favor­ite exper­i­ments inspire nearly as many new ques­tions as they answer. Next, we want to under­stand how and why one medick fam­ily escaped the tradeoff between mutu­al­ism and para­sit­ism. We can start to under­stand how it escaped by search­ing for genet­ic dif­fer­ences between it and the oth­er medick fam­il­ies in our exper­i­ment, to find the genes that help it build nod­ules without also form­ing galls.  We can also learn why it might have escaped the tradeoff by identi­fy­ing fea­tures that dis­tin­guish its home envir­on­ment from that of oth­er medicks.  For example, our escapee may come from an envir­on­ment where para­sit­ic nem­at­odes are hyper­abund­ant. In such an envir­on­ment, any medick with genes that allow it to form bac­teri­al nod­ules without also form­ing nem­at­ode galls is likely to out­com­pete its neighbors.

We sus­pect that the con­flict between attract­ing mutu­al­ists and repelling para­sites we dis­covered in medicks may be a common—but almost entirely overlooked—feature of spe­cies inter­ac­tions. If it is, it com­plic­ates how we think about the forces shap­ing res­ist­ance to para­sites and cooper­a­tion between mutu­al­ists. A tradeoff between mutu­al­ism and para­sit­ism could con­strain the evol­u­tion of para­site res­ist­ance by redu­cing the com­pet­it­ive advant­age of para­site-res­ist­ant indi­vidu­als. Wide­spread tradeoffs between mutu­al­ism and para­sit­ism may also explain why there so much vari­ation in mutu­al­ist qual­ity, when nat­ur­al selec­tion should oth­er­wise weed out unco­oper­at­ive partners.

And on a prac­tic­al level, under­stand­ing when and why para­site infec­tion is a col­lat­er­al cost of mutu­al­ism is an import­ant step towards safe­guard­ing the mutu­al­isms we rely on, from the bac­teria that nour­ish plants in our gar­dens to the microbes that live with­in our guts.

Dr Cor­lett Wolfe Wood is an EBB Postdoc­tor­al Fel­low at the Uni­ver­sity of Toronto. Her paper is freely avail­able to read and down­load in full from Evol­u­tion Let­ters here.

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