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Am­mo­nia-ox­id­iz­ing ar­chaea un­der the elec­tron mi­cro­scope. Credit: MARUM - Cen­ter for Mar­ine En­vir­on­mental Sci­ences, Uni­versity of Bre­men; M. Kön­neke.
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It was only re­l­at­ively re­cently that tiny, single-celled thau­marchaea were dis­covered to ex­ist and thrive in the pela­gic ocean, where their pop­u­la­tion size of roughly 1028 (10 bil­lion quin­til­lion) cells makes them one of the most abund­ant or­gan­isms on our planet. A team of re­search­ers from the Bio­logy Centre Czech Academy of Sci­ences (Bud­weis, Cze­chia), MARUM – Cen­ter for Mar­ine En­vir­on­mental Sci­ences at the Uni­versity of Bre­men, and Max Planck In­sti­tute for Mar­ine Mi­cro­bi­o­logy (Bre­men, Ger­many) have es­tim­ated that these chemoauto­trophs re­cycle ap­prox­im­ately 5 per cent of the car­bon and phos­phorus as­sim­il­ated by mar­ine al­gae and re­lease ter­ra­grams (1012 g) of dis­solved or­gan­ics to the ocean in­terior each year. These find­ings are now pub­lished in the journal Science Advances.

The wide­spread suc­cess of mar­ine thau­marchaea arises largely from their abil­ity to con­vert trace con­cen­tra­tions of am­mo­nia to ni­trite, which gives them en­ergy to fix car­bon and pro­duce new bio­mass in the ab­sence of light. This pro­cess, termed ni­tri­fic­a­tion, re­cycles the chem­ical en­ergy ori­gin­ally de­rived from pho­to­syn­thesis by mar­ine al­gae and is an es­sen­tial com­pon­ent of global nu­tri­ent cyc­ling. Us­ing a ra­dio­tracer ap­proach, the col­lab­or­at­ive re­search ef­fort has now de­term­ined that ar­chaea fix roughly 3 moles of car­bon for every 10 moles of am­mo­nia ox­id­ized and this ef­fi­ciency var­ies with cel­lu­lar ad­apt­a­tions to phos­phorus lim­it­a­tion.  “Thau­marchaea are act­ive throughout the ocean, and their vast num­bers im­ply sig­ni­fic­ant con­tri­bu­tions to global cycles of car­bon (C) and ni­tro­gen (N),” says Travis Meador, who is lead au­thor of the study and had re­ceived a grant by the Ger­man Re­search Found­a­tion (Deutsche Forschungs­ge­meinsch­aft DFG) to per­form this work dur­ing his time at MARUM. “Just how much car­bon is fixed by ni­tri­fi­ers is reg­u­lated by the amount of or­ganic ni­tro­gen (en­ergy) that is cre­ated dur­ing pho­to­syn­thesis, the physiolo­gical coup­ling of ni­tri­fic­a­tion and car­bon-as­sim­il­a­tion, and also ap­par­ently their abil­ity ac­cess to phos­phorus (P).”

Let them eat ammonia

Am­mo­nia in the ocean de­rives from the break­down of or­ganic mat­ter pro­duced by pho­to­trophs in sur­face wa­ters and is a valu­able source of en­ergy and nu­tri­tion for Eu­k­arya, Bac­teria, and Ar­chaea alike. Cul­ture stud­ies of the thau­marchaeon Nitrosopumilus maritimus have pre­vi­ously re­vealed that the tiny cells (Ø = 0.17-0.22 µm) boast en­zyme sys­tems to achieve a high af­fin­ity for am­mo­nia and the most en­ergy-ef­fi­cient C-fix­a­tion path­way in the pres­ence of oxy­gen. “These ad­apt­a­tions make thau­marchaea the oceans’ fore­most en­ergy re­cycler, al­low­ing them to out­com­pete their bac­terial coun­ter­parts and cre­ate a sep­ar­ate niche, par­tic­u­larly in the deep ocean where en­ergy is lim­it­ing,” Meador said. “Our col­leagues have sug­ges­ted that most or­ganic N that is ex­por­ted be­low the ocean’s eu­photic zone even­tu­ally fuels ni­tri­fic­a­tion by thau­marchaea. While the global ex­port flux has been in­vest­ig­ated for sev­eral dec­ades, there has been no em­pir­ical evid­ence to fur­ther couple ar­chaeal am­mo­nia ox­id­a­tion to global rates of C-fix­a­tion, un­til now.”

The need for P

In ad­di­tion to their im­port­ant con­tri­bu­tions to chem­ical fluxes in the dark ocean chem­ical, thau­marchaea are ac­tu­ally more abund­ant in the eu­photic zone, where the ma­jor­ity of or­ganic mat­ter is respired (to CO2 and am­mo­nia). In fact, the highest ac­cu­mu­la­tions of am­mo­nia may be situ­ated at the base of the eu­photic zone, where het­ero­trophic bac­teria feed on the sink­ing bio­mass pro­duced in the warm, sur­face mixed-layer and be­low where wa­ter tem­per­at­ures de­crease rap­idly with depth.

This zone, known as the ther­mo­cline, also ex­per­i­ences large fluc­tu­ations in the con­cen­tra­tion and turnover time of an­other key nu­tri­ent, phos­phate (P). The re­search­ers thus ques­tioned if thau­marchaeal ac­cess to phos­phate may con­trol their con­tri­bu­tions to re­cycled pro­duc­tion in the sur­face ocean.

Interrogating archaea with radioactivity

By in­tro­du­cing ra­diolabeled 14C-bi­car­bon­ate and 33P-phos­phate to the cul­ture me­dium, the au­thors could track the rates of C and P as­sim­il­ated into N. maritimus cells and re­leased as dis­solved or­ganic car­bon and phos­phorus (DOC and DOP) meta­bol­ites into cul­ture me­dia. Nor­mal­iz­ing these rates to ni­tri­fic­a­tion, the re­search­ers gen­er­ated the first es­tim­ates of C-, P-, DOC-, and DOP- yields for a mar­ine ar­chaeon.

Acquainting the models

The up­shot of this work is that global rates of C-fix­a­tion by widely-dis­trib­uted thau­marchaea are likely at least 3-fold higher than pre­vi­ously as­sumed. Also, C- and P-as­sim­il­a­tion by mar­ine ar­chaea may now be modeled as dir­ectly pro­por­tional to the renowned re­min­er­al­iz­a­tion ra­tio es­tab­lished by Al­fred Red­field in the mid-20th cen­tury. The re­search­ers fur­ther found that N. maritimus is apt at ac­quir­ing phos­phate, but stra­tegic in­creases in cel­lu­lar phos­phate af­fin­ity came at a cost of ap­prox­im­ately 30 per cent re­duc­tion in C-fix­a­tion ef­fi­ciency. These res­ults may there­fore ex­plain the widely ran­ging val­ues of spe­cific ni­tri­fic­a­tion rate ob­served across the sur­face ocean. Fi­nally, Meador por­tends that “the re­lease of chemo­syn­thet­ic­ally man­u­fac­tured com­pounds by thau­marchaea is minor com­pared to the sub­stan­tial reser­voir of dis­solved or­ganic nu­tri­ents in the ocean, but it does rep­res­ent a fresh flux of labile sub­strates throughout the ocean in­terior”.

Travis B. Meador, Niels Schof­felen, Timothy G. Fer­del­man, Os­mond Re­bello, Al­ex­an­der  Khachikyan, Mar­tin Kön­neke: Car­bon re­cyc­ling ef­fi­ciency and phos­phate turnover by mar­ine ni­tri­fy­ing ar­chaea. Sci­ence Ad­vances 2020. DOI: 10.1126/sciadv.aba1799.

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