Something Old, Something New in the Ocean`s Blue

The dis­cov­ery of an unknown meta­bolic path­way adds a new di­men­sion to the global car­bon cycle

Microbiologists at the Max Planck Institutes in Marburg and Bremen have discovered a new metabolic process in the ocean. Ranging from molecular structures of individual genes and detection of their global distribution, their results give insight into the pathway process and its degradation products and thus provide valuable information for future calculations of the ocean`s carbon dioxide balance.

Charles Dar­win sus­pec­ted something in the "clear blue wa­ter" of the ocean that was even smal­ler than the pro­to­zoa he could see un­der the mi­cro­scope. "Today we know that every liter of ocean wa­ter is swarm­ing with hun­dreds of mil­lions of mi­croor­gan­isms," ex­plains mar­ine re­searcher Rudolf Amann, Dir­ector at the Max Planck In­sti­tute for Mar­ine Mi­cro­bi­o­logy in Bre­men. His col­league To­bias Erb from the sis­ter in­sti­tute of ter­restrial Mi­cro­bi­o­logy in Mar­burg adds: "Al­though only mi­cro­met­ers in size, the mi­croor­gan­isms with their sheer num­ber and high rate of meta­bol­ism have a strong im­pact on en­ergy flow and bio­mass turnover in the oceans.”

Whilst the uni­cel­lu­lar al­gae, also known as phyto­plank­ton, con­vert CO2 into bio­mass, other mi­croor­gan­isms come onto ac­tion when the al­gae ex­crete the fixed car­bon - either dur­ing their life, or when they die - some­times in mass, as after the so-called al­gae bloom. Even in sur­face wa­ter, single-cell or­gan­isms pro­cess many thou­sands of tons of al­gae bio­mass: a cent­ral pro­cess in the mar­ine life cycle. One of the most im­port­ant com­pounds in the ocean is glycolic acid, a dir­ect by-product of pho­to­syn­thesis that is partly con­ver­ted back into CO2 by mar­ine bac­teria. But here, the pic­ture be­comes blurred - the ex­act fate of the car­bon in glycolic acid was un­known so far.

IIn or­der to come to gain a use­ful as­sess­ment of the global car­bon cycle, however, the equa­tion must not have too many un­knowns. As we know today, too much CO2 in­flu­ences life in the ocean. In­creased con­cen­tra­tions of CO2 in sea­wa­ter acid­ify the oceans, dis­turb the bal­ance between phyto­plank­ton and mi­croor­gan­isms and ul­ti­mately in­flu­ence global cli­mate. In or­der to un­der­stand the con­sequences for cli­mate change on a global scale, a pre­cise know­ledge of the bac­terial de­grad­a­tion of al­gae bio­mass is in­dis­pens­able. For this, however, we need pre­cise ba­sic know­ledge of the loc­a­tion, rate and ex­tent of nu­tri­ent net­works in the ocean. So what ex­actly is the fate of the glycolic acid`s car­bon, which glob­ally means sub­stance quant­it­ies in the range of one bil­lion tons per year?

The forgotten pathway

Re­search­ers do not al­ways have to start from scratch - some­times there are already known puzzle pieces, they just have to be re­cog­nized and placed cor­rectly. One such piece is the β-hy­droxy­as­part­ate cycle. It was dis­covered more than 50 years ago in the soil bac­terium Paracoccus. At that time, the meta­bolic path­way re­ceived little at­ten­tion and its ex­act bio­chem­ical pro­cesses re­mained un­ex­plored. Dr. Len­nart Schada von Borzyskowski, first au­thor of the cur­rent Nature pub­lic­a­tion, is a postdoc­toral fel­low in To­bias Er­b's de­part­ment at the Max Planck In­sti­tute for Ter­restrial Mi­cro­bi­o­logy in Mar­burg, dis­covered this meta­bolic path­way in the course of lit­er­at­ure re­search. "Look­ing at this meta­bolic path­way, I no­ticed that it should be more ef­fi­cient than the pro­cess pre­vi­ously as­sumed for the de­grad­a­tion of glycolic acid, and I wondered whether it might be more im­port­ant than ori­gin­ally as­sumed," the sci­ent­ist re­ports.

In the 70,000 square kilometer wide German Bight alone, an algal bloom produces about ten million tones of biomass each spring.
(© NASA)

Equipped with only a single gene se­quence, he came across a cluster of four genes in data­bases that provided the con­struc­tion in­struc­tions for four en­zymes. In com­bin­a­tion, three of the en­zymes were suf­fi­cient to pro­cess a com­pound de­rived from glycolic acid. But what was the fourth en­zyme re­spons­ible for? Schada von Borzyskowski tested this en­zyme in the labor­at­ory and dis­covered that it cata­lyzed an imine re­ac­tion pre­vi­ously un­known in this con­text. This fourth re­ac­tion closes the meta­bolic path­way to an el­eg­ant cycle through which the car­bon of glycolic acid can be re­cycled without the loss of CO2.

Globally distributed, ecologically significant

A co­oper­a­tion with sci­ent­ists from the Uni­versity of Mar­burg made it pos­sible to study the glycolic acid meta­bol­ism and its reg­u­la­tion in liv­ing mi­croor­gan­isms. "Now our task was to look for the pres­ence and activ­ity of these genes in mar­ine hab­it­ats and their eco­lo­gical sig­ni­fic­ance," To­bias Erb ex­plains. The co­oper­a­tion between the Mar­burg bio­chem­ists and the mar­ine re­search­ers at the Max Planck In­sti­tute in Bre­men proved to be highly fruit­ful, as the lat­ter have been study­ing the mar­ine com­munit­ies near Hel­go­land for years, in par­tic­u­lar the bac­terial pop­u­la­tions dur­ing and after algal blooms. In sev­eral ex­cur­sions on the high seas, the sci­ent­ists from Mar­burg and Bre­men meas­ured form­a­tion and con­sump­tion of glycolic acid dur­ing algal bloom in spring 2018. In­deed: the meta­bolic cycle was act­ively in­volved in the meta­bol­ism of glycolic acid.

The blue­prints of the meta­bolic cycle also were found re­peatedly in the bac­terial gen­ome se­quences that the TARA Oceans expedition had col­lec­ted from the world's oceans over a dis­tance of 10,000 kilo­met­ers, with a on av­er­age 20 times higher pre­val­ence than all other pos­tu­lated de­grad­a­tion routes for glycolic acid.

Microbial research ranged from unraveling molecular principles in the laboratory to verifying their significance for the marine ecosystem.
Credit: © Max Planck Institute for Marine Microbiology/ G. Gerdts

Thus the re­dis­covered meta­bolic path­way is not a niche ex­ist­ence, but on the con­trary wide­spread. These new find­ings still amaze Rudolf Amann: "The dis­cov­ery of our col­leagues in Mar­burg turns our pre­vi­ous un­der­stand­ing of the fate of glycolic acid up­side down. Our data show that we have to re­as­sess the cycle of bil­lions of tons of car­bon in the oceans." As To­bias Erb con­tin­ues: "This work makes us aware of the global di­men­sions of the meta­bol­ism of mi­croor­gan­isms, and at the same time it shows us how much we still have to dis­cover to­gether.”

Contacts and sources:
Dr. Fanni Aspetsberger
MPI for Marine Microbiology

Dr. Fanni Aspetsberger
MPI for Marine Microbiology
Max Planck Institute for Marine Microbiology

 Prof. Dr. Tobias Erb
Max Planck In­sti­tut for ter­restrial Mi­cro­bi­o­logy, Mar­burg

Citation:  Marine Proteobacteria metabolize glycolate via the β-hydroxyaspartate cycle. Lennart Schada von Borzyskowski, Francesca Severi, Karen Krüger, Lucas Hermann, Alexandre Gilardet, Felix Sippel, Bianca Pommerenke, Peter Claus, Niña Socorro Cortina, Timo Glatter, Stefan Zauner, Jan Zarzycki, Bernhard M. Fuchs, Erhard Bremer, Uwe G. Maier, Rudolf I. Amann, Tobias J. Erb. Nature, 2019; DOI: 10.1038/s41586-019-1748-4


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