Five Ques­tions About Oomycetes

We re­cently reprinted an ar­ti­cle by Patrick Keel­ing en­ti­tled Five Ques­tions About Mi­crosporidia. His fine dis­cussion prompted us to at­tempt a sim­i­lar ex­am­i­na­tion of an­other highly im­por­tant – but oft-ne­glected – group of mi­crobes, the oomycetes or wa­ter molds. We will post three ar­ti­cles, the first one (here­with) describ­ing oomycete bi­ol­ogy, the other two fo­cus on a par­tic­u­lar oomycete: the late potato blight pathogen. There we will re­count a bit of Irish his­tory and then dis­cuss as­pects of the pathogen's genome.

by Elio

What Makes Oomycetes Im­por­tant to Peo­ple?

As you know, the potato blight caused wide­spread fa­mi­ne in potato-de­pen­dent, mid-19th cen­tury Ire­land. You may also be aware of a cur­rent mal­ady, sud­den oak death, that af­fects large num­bers of trees in the Pa­cific coastal states of the USA. And if you are in­volved in ag­riculture in any way, you have likely heard of the downy mildews of let­tuce, onions, spinach, straw­ber­ries, and other crops. Like­wise, those con­cerned with aqua­cul­ture are alert to a va­ri­ety of "fun­gal" dis­eases, in­clud­ing one called sapro­leg­ni­a­sis that causes about a 10% mor­tal­ity in pond-grown salmon.

Koi carp in­fec­tion by Sapro­leg­nia. Source

What do these dis­eases have in com­mon? They are all caused by oomycetes, a large group of or­ganisms that re­sem­ble fungi mor­pho­log­i­cally but are dis­tant from them phy­lo­ge­net­i­cally. Patho­genic oomycetes cause mas­sive de­struc­tion and huge losses in agri­cul­ture and aqua­cul­ture. They in­fect many an­i­mals, among them fish, cray­fish, and mam­mals – in­clud­ing hu­mans. Oomycetes, along with chytrid fungi, are thought to be in­volved in the cur­rent global de­cline of the frog popu­lations. Since some oomycetes prey on path­o­genic fungi, they are con­sid­ered can­di­dates for bio­logical con­trol of fun­gal in­fec­tions of plants.

Be­cause of their im­pact, much ef­fort has been de­voted to elu­ci­dat­ing the ge­net­ics and biochemis­try of par­tic­u­lar oomycetes. Likely the best stud­ied one is the agent of the potato blight, Phytoph­thora in­fes­tans. The lit­er­a­ture about this or­gan­ism is in­deed im­pres­sive, com­men­su­rate with this organism's ac­com­plish­ments as a pathogen.

Are Oomycetes Fungi or What?

Oomycetes are a di­verse group of eu­kary­otic or­gan­isms. The 500 or so species in­clude both pa­rasites and saprobes. They are found world­wide in fresh­wa­ter and ma­rine habi­tats. Some pre­fer well-aer­ated streams, oth­ers stag­nant wa­ters.

The oomycetes in the Tree of Life. Source

They have been tra­di­tion­ally lumped with the fungi, part­ly be­cause, be­ing fil­a­men­tous, they look like fil­a­men­tous fungi. When grown on agar, it can be hard to tell the two groups apart – they both make hy­phae and mycelia. Oo­my­cetes and fungi share a nu­tri­tional mode: they feed by se­cret­ing en­zymes that de­grade poly­mers such as cellu­lose, lipids, and pro­teins, then im­port the re­sult­ing build­ing blocks into their own grow­ing cells. Like fungi, oomy­cetes re­pro­duce by both sex­ual and asex­ual spores. But are they kin? Mol­e­c­u­lar phy­logeny places them in a to­tally dif­fer­ent king­dom, the stra­menopiles (aka hetero­konts).

So what are stra­menopiles? They are a large group of pro­tists (over 100,000 species) that in­clude many pre­vi­ously clas­si­fied as fungi, pro­to­zoa, or al­gae (such as di­atoms and kelp). The oomycetes com­prise the largest group of non-pho­to­syn­the­siz­ing stra­menopiles. Stra­menopiles share some dis­tin­guish­ing struc­tural fea­tures, such as tubu­lar cristae in their mi­to­chon­dria and motile asex­ual spores. These zoospores have two fla­gella: the an­te­rior one is called a "tin­sel" fla­gel­lum for its nu­merous hair-like pro­jec­tions along the shaft; the pos­te­rior one is termed a "whiplash" fla­gel­lum. The an­te­rior fla­gel­lum is prob­a­bly re­spon­si­ble for pulling the zoospore through the wa­ter, while the pos­te­rior one acts as a rud­der for steer­ing the cell. Tax­on­o­mists get ex­cited about these defin­ing struc­tural char­ac­ter­is­tics. Zoospores are wall-less, thus are sen­si­tive to cer­tain en­vi­ron­men­tal chal­lenges.

The oomycete life cy­cle. Source (Exam2 Figure8­Life­cy­cle.jpg)

There are other ways that you can tell an oomycete from a fun­gus. Oomycetes are diploid for most of their life cy­cle, fungi mainly hap­loid. The two groups syn­the­size ly­sine by dif­fer­ent path­ways (fungi via α‑aminoadipic acid, oomycetes via α,ε‑diaminopimelic acid). The cell walls of fungi con­tain chitin in high amounts, those of oomycetes are made up of other glu­cans, in­clud­ing cel­lu­lose.

Al­though the oomycetes and the fungi are un­re­lated, their many phe­no­typic sim­i­lar­i­ties bring to mind thoughts of con­ver­gent evo­lu­tion. Re­cently it was found that oomycetes have ac­quired some genes from fungi, but they have also im­ported genes from di­atoms, brown al­gae, and even cyanobac­te­ria. Such gene trans­fer events ap­pear to have taken place of­ten, sug­gest­ing that the oo­mycete genome has a chimeric an­ces­try.

De­spite all their phy­lo­ge­netic and phys­i­o­log­i­cal dif­fer­ences, the fact re­mains that oomycetes look a lot like fil­a­men­tous fungi. This is one of those sit­u­a­tions where mol­e­c­u­lar and bio­chem­i­cal facts don't match up with what your senses (com­mon or oth­er­wise) tell you. We re­peat the words of Grou­cho Marx: Who are you go­ing to be­lieve, me or your own eyes?

What Does Oomycete Mean?

It means "egg fun­gus," a term coined be­cause of the large round struc­tures con­tain­ing the fe­male ga­metes, the oogo­nia. The other com­mon name for some oomycetes, "wa­ter molds," refers to the fact that they were first found in fresh­wa­ter habi­tats.

The case has been made that the fa­mil­iar term "fun­gus" should not be lim­ited to strictly systemati­cally cor­rect us­age. The dis­tin­guished my­col­o­gist Nik Money sug­gests that, de­spite the phyloge­ne­tic chasm be­tween the fungi and the oomycetes, "egg fun­gus" is an ac­cept­able col­lo­quial us­age that ben­e­fits from the all-em­brac­ing con­no­ta­tion of "fun­gus." Do you think this is go­ing to fly? On the other hand, the term "mold" lacks a spe­cific phy­lo­ge­netic as­so­ci­a­tion, and thus one can use "wa­ter molds" in even the best tax­o­nomic com­pany.

What Is the Life Cy­cle of Oomycetes?

Oomycetes are diploid through­out their life cy­cle, ex­cept briefly when they are hap­loid gametes—just like us. In the asex­ual cy­cle, hy­phae dif­fer­en­ti­ate into struc­tures called spo­ran­gia that con­tain the motile zoospores. This process has been stud­ied in some de­tail; some sporu­la­tion-spe­cific genes have been iden­ti­fied and their role in dif­fer­en­ti­a­tion elu­ci­dated. The zoospores ger­mi­nate to make more hy­phae, which make more spores, and so on. When zoospores of some species ger­mi­nate, they give rise to two kinds of hy­phae, male and fe­male.

SEM of a zy­gote (oocyte) in the mak­ing. The round, sphe­rical cell is the fe­male oogo­nium, the swollen hy­pha, the male an­theridium. Source

The sex­ual cy­cle gets go­ing when ter­mi­nal cells in the hy­phae un­dergo meio­sis and dif­fer­en­ti­ate into hap­loid ga­metes, some male and oth­ers fe­male. We usu­ally think of ga­metes as be­ing free cells, but these are not. Rather they re­main at­tached to their parental hy­phae. The cell car­ry­ing the fe­male ga­mete (oogo­nium) is spher­i­cal, whereas the one with the male ga­mete (an­therid­ium) looks pretty much like a reg­u­lar but swollen hy­phal cell. The two mate via a fer­til­iza­tion tube ex­tend­ing from the male to the fe­male ga­mete, which gives rise to the zy­gote, the oocyte. Even­tu­ally the zy­gote ger­mi­nates to yield more hy­phae. Mat­ing types and com­pat­i­bil­ity are also part of the sex­ual story. Un­like the zoospores, oospores (de­rived from the oocytes) are highly re­sis­tant to des­ic­ca­tion and other en­vi­ron­men­tal in­flu­ences – thus im­por­tant in the trans­mis­sion of these or­gan­isms be­tween hosts. Sex among the oomycetes plays an ex­tra, un­usual role: it is part of their strat­egy for sur­vival.

How Do Oomycetes In­fect Their Hosts?

Many, per­haps most, of path­o­genic oomycetes have a broad host range, mean­ing that they in­fect a va­ri­ety of species. Thus, Sapro­leg­nia par­a­sit­ica causes lethal in­fec­tions of bass, trout, cat­fish, bream, floun­der, and other fresh­wa­ter fish. The agent of Sud­den Oak death, Phy­toph­thora ramo­rum, causes se­ri­ous dis­ease not only in oaks but also in red­woods, Dou­glas firs, and other trees. And Pythium in­sidio­sum causes chronic skin le­sions in a large va­ri­ety of mam­mals, in­clud­ing do­mestic an­i­mals and hu­mans.

Early stages of downy mildew in­fec­tion. A spore ger­minates to pro­duce a germ tube and ap­pres­so­rium. The hy­phae grow and make haus­to­ria that in­vade the host cells. Source: Uni­ver­sity of Utrecht, Downy Mildew Ge­nomics

The best stud­ied of the path­o­genic oomycetes is Phyto­phthora in­fes­tans, the agent of potato blight and sim­i­lar dis­eases in re­lated plants. In­fec­tion of hosts is of­ten the work of the motile zoospores that are pro­duced in large num­bers from the spo­ran­gia. They find their hosts by chemo­tac­ti­cally sens­ing chem­i­cals se­creted by the plants. Once in con­tact with the host, zoospores turn into resis­tant cysts that turn into hy­phae. Oomycete hy­phae and their spe­cial­ized forms, the haus­to­ria, do not pen­e­trate the plant cells but ob­tain nu­tri­ents from chem­i­cals se­creted by the plant. The oomycete stim­u­lates this pro­cess by it­self se­cret­ing cer­tain pro­teins. The necro­sis in the plant leaves is due to a hy­per­sen­si­tiv­ity re­ac­tion that rec­og­nizes the pathogen's at­tack.

The hy­phae spread in all di­rec­tions, even­tu­ally caus­ing a vis­i­ble necrotic le­sion. Other path­o­genic oomycetes cause dis­ease by us­ing vari­a­tions on this theme. How­ever they do it, they are, in the words of the British oomycete ex­pert Gor­don Beakes, "nat­ural born killers."

Click here (sorry, link is dead as of 2021) for a movie of Phy­toph­thora so­jae (a soy­bean pathogen) spo­rangium ger­mi­na­tion and zoospore re­lease. Credit: Ed­ward Braun

There is even more drama to be found among the oomy­cetes. Some are able to forcibly dis­charge spores into a po­ten­tial host. We pre­vi­ously fea­tured one, Hap­toglossa, with its highly dif­fer­en­ti­ated gun cells ca­pa­ble of in­ject­ing a vi­able spore into pass­ing ne­ma­todes or other hosts. (There we called it a fun­gus, dis­play­ing our pre­vi­ous igno­rance and the tax­o­nomic con­fu­sion wide­spread in the field.) Note that sim­i­lar mech­a­nisms of spore dis­charge are used by the mi­crosporidia.

We can un­der­stand why enig­matic and con­fus­ing groups, such as the mi­crosporidia and the oo­mycetes, have of­ten been ig­nored in fa­vor of oth­ers. But this has been our loss, as they are fas­ci­nat­ing.

I thank Nik Money for help­ful sug­ges­tions. I also thank Matthew Mar­tin for cor­rect­ing some mis­in­for­ma­tion that crept into a pre­vi­ous ver­sion of this post.