Mud pots in Solfatara
NEWS | 15.09.2020

When meth­ane-eat­ing mi­crobes eat am­mo­nia in­stead

As a side effect of their metabolism, microorganisms living on methane can also convert ammonia. In the process, they produce nitric oxide (NO), a central molecule in the global nitrogen cycle. Scientists from the Max Planck Institute for Marine Microbiology, Bremen (DE), a member of the German Marine Research Alliance (Deutsche Allianz Meeresforschung, DAM), and Radboud University, Nijmegen (NL), now discovered the enzyme that produces NO, closing an important gap in our understanding of how methanotrophs deal with rising environmental ammonia concentrations.

Some mi­croor­gan­isms, the so-called meth­an­o­trophs, make a liv­ing by ox­id­iz­ing meth­ane (CH4) to car­bon di­ox­ide (CO2). Am­mo­nia (NH3) is struc­tur­ally very sim­ilar to meth­ane, thus meth­an­o­trophs also co-meta­bol­ize am­mo­nia and pro­duce ni­trite. While this pro­cess was ob­served in cell cul­tures, the un­der­ly­ing bio­chem­ical mech­an­ism was not un­der­stood. Boran Kartal, head of the Microbial Physiology Group at the Max Planck Institute for Marine Microbiology in Bre­men, Ger­many, and a group of sci­ent­ists from Rad­boud Uni­versity in Nijme­gen, The Neth­er­lands, now shed light on an ex­cit­ing miss­ing link in the pro­cess: the pro­duc­tion of nitric ox­ide (NO).

Nitric ox­ide is a highly re­act­ive and toxic mo­lecule with fas­cin­at­ing and ver­sat­ile roles in bio­logy and at­mo­spheric chem­istry. It is a sig­nal­ing mo­lec­ule, the pre­cursor of the po­tent green­house gas ni­trous ox­ide (N2O), de­pletes the ozone layer in our at­mo­sphere, and a key in­ter­me­di­ate in the global ni­tro­gen cycle. It now turns out that NO is also the key for the sur­vival of meth­an­o­trophs that face am­mo­nia in the en­vir­on­ment – which they do more and more as fer­til­izer in­put into nature in­creases. When meth­an­o­trophs co-meta­bol­ize am­mo­nia they ini­tially pro­duce hy­droxylam­ine, which in­hib­its other im­port­ant meta­bolic pro­cesses, res­ult­ing in cell death. Thus, meth­an­o­trophs need to get rid of hy­droxylam­ine as fast as pos­sible. “Car­ry­ing a hy­droxylam­ine-con­vert­ing en­zyme is a mat­ter of life or death for meth­ane-eat­ing mi­crobes”, Kartal says.

For their study, Kartal and his col­leagues used a meth­an­o­trophic bac­terium named Methylacidiphilum fumariolicum, which ori­gin­ates from a vol­canic mud pot, char­ac­ter­ized by high tem­per­at­ures and low pH, in the vi­cin­ity of Mount Vesuvius in Italy. “From this mi­crobe, we pur­i­fied a hy­droxylam­ine ox­idore­ductase (mHAO) en­zyme,“ re­ports Kartal. “Pre­vi­ously it was be­lieved that mHAO en­zyme would ox­id­ize hy­droxylam­ine to ni­trite in meth­an­o­trophs. We now showed that it ac­tu­ally rap­idly pro­duces NO.” The mHAO en­zyme is very sim­ilar to the one used by “ac­tual” am­mo­nia ox­id­izers, which is quite as­ton­ish­ing, as Kartal ex­plains: “It is now clear that en­zymat­ic­ally there is not much dif­fer­ence between aer­obic am­mo­nia- and meth­ane-ox­id­iz­ing bac­teria. Us­ing es­sen­tially the same set of en­zymes, meth­an­o­trophs can act as de facto am­mo­nia ox­id­izers in the en­vir­on­ment. Still, how these mi­crobes ox­id­ize NO fur­ther to ni­trite re­mains un­known.”

The ad­apt­a­tion of the mHAO en­zyme to the hot vol­canic mud pots is also in­triguing, Kartal be­lieves: “At the amino acid level, the mHAO and its coun­ter­part from am­mo­nia ox­id­izers are very sim­ilar, but the pro­tein we isol­ated from M. fumariolicum thrives at tem­per­at­ures up to 80 °C, al­most 30 °C above the tem­per­at­ure op­timum of their “ac­tual” am­mo­nia-ox­id­iz­ing re­l­at­ives. Un­der­stand­ing how so sim­ilar en­zymes have such dif­fer­ent tem­per­at­ure op­tima and range will be very in­ter­est­ing to in­vest­ig­ate.”

Ac­cord­ing to Kartal, pro­duc­tion of NO from am­mo­nia has fur­ther im­plic­a­tions for meth­ane-eat­ing mi­crobes: “Cur­rently there are no known meth­an­o­trophs that can make a liv­ing out of am­mo­nia ox­id­a­tion to ni­trite via NO, but there could be meth­an­o­trophs out there that found a way to con­nect am­mo­nia con­ver­sion to cell growth.”

Ori­ginal pub­lic­a­tion:

Wouter Versant­voort, Ar­jan Pol, Mike S. M. Jetten, Laura van Niftrik, Joachim Re­imann, Boran Kartal, and Huub J. M. Op den Camp: Multiheme hydroxylamine oxidoreductases produce NO during ammonia oxidation in methanotrophs. PNAS. Septem­ber 2020.
DOI: 10.1073/pnas.2011299117

Contacts:
Dr. Boran Kartal
Group leader Microbial Physiology Research Group
Max Planck In­sti­tute for Mar­ine Mi­cro­bi­o­logy
+49 421 2028-645
bkar­tal(at)mpi-bre­men.de

Dr. Fanni Aspetsberger
Head of Press & Communications
Max Planck In­sti­tute for Mar­ine Mi­cro­bi­o­logy
+49 421 2028-947
fas­petsb(at)mpi-bre­men.de

Photo: Patrick Massot

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