Metabolite release by nitrifiers facilitates metabolic interactions in the ocean

Bayer, Barbara; Liu, Shuting; Louie, Katherine; Northen, Trent R.; Wagner, Michael; Daims, Holger; Carlson, Craig A.; Santoro, Alyson E.

doi:10.1093/ismejo/wrae172

Metabolite release by nitrifiers facilitates metabolic interactions in the ocean

Journal Article · Sun Sep 08 00:00:00 EDT 2024 · The ISME Journal

DOI:https://doi.org/10.1093/ismejo/wrae172· OSTI ID:2476188

Bayer, Barbara ^[1]; Liu, Shuting ^[2]; Louie, Katherine ^[3]; Northen, Trent R. ^[3]; Wagner, Michael ^[4]; Daims, Holger ^[5]; Carlson, Craig A. ^[6]; Santoro, Alyson E. ^[6]

Univ. of Vienna (Austria); Univ. of California, Santa Barbara, CA (United States)
Univ. of California, Santa Barbara, CA (United States); Kean University, Union, NJ (United States)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Univ. of Vienna (Austria); Aalborg Univ. (Denmark)
Univ. of Vienna (Austria)
Univ. of California, Santa Barbara, CA (United States)

Microbial chemoautotroph-heterotroph interactions may play a pivotal role in the cycling of carbon in the deep ocean, reminiscent of phytoplankton-heterotroph associations in surface waters. Nitrifiers are the most abundant chemoautotrophs in the global ocean, yet very little is known about nitrifier metabolite production, release, and transfer to heterotrophic microbial communities. To elucidate which organic compounds are released by nitrifiers and potentially available to heterotrophs, we characterized the exo- and endometabolomes of the ammonia-oxidizing archaeon Nitrosopumilus adriaticus CCS1 and the nitrite-oxidizing bacterium Nitrospina gracilis Nb-211. Nitrifier endometabolome composition was not a good predictor of exometabolite availability, indicating that metabolites were predominately released by mechanisms other than cell death/lysis. Although both nitrifiers released labile organic compounds, N. adriaticus preferentially released amino acids, particularly glycine, suggesting that its cell membranes might be more permeable to small, hydrophobic amino acids. We further initiated co-culture systems between each nitrifier and a heterotrophic alphaproteobacterium, and compared exometabolite and transcript patterns of nitrifiers grown axenically to those in co-culture. In particular, B vitamins exhibited dynamic production and consumption patterns in nitrifier-heterotroph co-cultures. We observed an increased production of vitamin B₂ and the vitamin B₁₂ lower ligand dimethylbenzimidazole by N. adriaticus and N. gracilis, respectively. In contrast, the heterotroph likely produced vitamin B₅ in co-culture with both nitrifiers and consumed the vitamin B₇ precursor dethiobiotin when grown with N. gracilis. Our results indicate that B vitamins and their precursors could play a particularly important role in governing specific metabolic interactions between nitrifiers and heterotrophic microbes in the ocean.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Joint Genome Institute (JGI); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2476188

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 1 Vol. 18; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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54 ENVIRONMENTAL SCIENCES
Nitrosopumilus
Nitrospina
chemoautotroph-heterotroph associations
metabolomics
microbial interactions
nitrifier metabolite release
transcriptomics

Metabolite release by nitrifiers facilitates metabolic interactions in the ocean

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