Carbon content, carbon fixation yield and dissolved organic carbon release from diverse marine nitrifiers

Barbara Bayer; Kelsey McBeain; Craig A. Carlson; Alyson E. Santoro

doi:10.1002/lno.12252

Carbon content, carbon fixation yield and dissolved organic carbon release from diverse marine nitrifiers

Barbara Bayer (Corresponding author)
, Kelsey McBeain
, Craig A. Carlson
, Alyson E. Santoro

Publications: Contribution to journal › Article › Peer Reviewed

Abstract

Nitrifying microorganisms, including ammonia-oxidizing archaea, ammonia-oxidizing bacteria, and nitrite-oxidizing bacteria, are the most abundant chemoautotrophs in the ocean and play an important role in the global carbon cycle by fixing dissolved inorganic carbon (DIC) into biomass. The release of organic compounds by these microbes is not well quantified, but may represent an as-yet unaccounted source of dissolved organic carbon (DOC) available to marine food webs. Here, we provide measurements of cellular carbon and nitrogen quotas, DIC fixation yields and DOC release of 10 phylogenetically diverse marine nitrifiers. All investigated strains released DOC during growth, representing on average 5-15% of the fixed DIC. Changes in substrate concentration and temperature did not affect the proportion of fixed DIC released as DOC, but release rates varied between closely related species. Our results also indicate previous studies may have underestimated DIC fixation yields of marine nitrite oxidizers due to partial decoupling of nitrite oxidation from CO2 fixation, and due to lower observed yields in artificial compared to natural seawater medium. The results of this study provide critical values for biogeochemical models of the global carbon cycle, and help to further constrain the implications of nitrification-fueled chemoautotrophy for marine food-web functioning and the biological sequestration of carbon in the ocean.

Original language	English
Pages (from-to)	84-96
Number of pages	13
Journal	Limnology and Oceanography
Volume	68
Issue number	1
Early online date	27 Oct 2022
DOIs	https://doi.org/10.1002/lno.12252
Publication status	Published - 1 Jan 2023
Externally published	Yes

Funding

We thank Thomas Reinthaler for advice on DIC fixation measurements and for sharing his lab protocols, and Elisa Halewood and Janice Jones for support and advice with setting up the DIC fixation method in the lab. We also thank Sylvia Kim for total alkalinity and pH measurements, Keri Opalk for TOC measurements, Kenneth Marchus for elemental (CHN) analyses, Christopher Sedlacek for sending culture stocks of Nitrosopumilus adriaticus and Nitrosopumilus piranensis, Claus Pelikan for advice on statistical analyses, and Holger Daims for advice on bioenergetic considerations. Frederica Valois and John B. Waterbury are acknowledged for their decades-long commitment and maintenance of the nitrifier culture collection at the Woods Hole Oceanographic Institution. This research was supported by a Simons Foundation Early Career Investigator in Marine Microbiology and Evolution Award (345889) and a US National Science Foundation (NSF) award OCE-1924512 to AES. BB was supported by the Austrian Science Fund (FWF) Project Number: J4426-B ("The influence of nitrifiers on the oceanic carbon cycle"). Support for CAC was provided by Simons Foundation International's PBIOS-SCOPE program.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 14 Life Below Water

Austrian Fields of Science 2012

106022 Microbiology

Keywords

AMMONIA-OXIDIZING BACTERIA
NITRITE-OXIDIZING BACTERIA
AMMONIA-OXIDIZING ARCHAEA
MARINE
NITRIFICATION
CARBON FIXATION
DOC RELEASE

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Cite this

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title = "Carbon content, carbon fixation yield and dissolved organic carbon release from diverse marine nitrifiers",

abstract = "Nitrifying microorganisms, including ammonia-oxidizing archaea, ammonia-oxidizing bacteria, and nitrite-oxidizing bacteria, are the most abundant chemoautotrophs in the ocean and play an important role in the global carbon cycle by fixing dissolved inorganic carbon (DIC) into biomass. The release of organic compounds by these microbes is not well quantified, but may represent an as-yet unaccounted source of dissolved organic carbon (DOC) available to marine food webs. Here, we provide measurements of cellular carbon and nitrogen quotas, DIC fixation yields and DOC release of 10 phylogenetically diverse marine nitrifiers. All investigated strains released DOC during growth, representing on average 5-15\% of the fixed DIC. Changes in substrate concentration and temperature did not affect the proportion of fixed DIC released as DOC, but release rates varied between closely related species. Our results also indicate previous studies may have underestimated DIC fixation yields of marine nitrite oxidizers due to partial decoupling of nitrite oxidation from CO2 fixation, and due to lower observed yields in artificial compared to natural seawater medium. The results of this study provide critical values for biogeochemical models of the global carbon cycle, and help to further constrain the implications of nitrification-fueled chemoautotrophy for marine food-web functioning and the biological sequestration of carbon in the ocean.",

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AB - Nitrifying microorganisms, including ammonia-oxidizing archaea, ammonia-oxidizing bacteria, and nitrite-oxidizing bacteria, are the most abundant chemoautotrophs in the ocean and play an important role in the global carbon cycle by fixing dissolved inorganic carbon (DIC) into biomass. The release of organic compounds by these microbes is not well quantified, but may represent an as-yet unaccounted source of dissolved organic carbon (DOC) available to marine food webs. Here, we provide measurements of cellular carbon and nitrogen quotas, DIC fixation yields and DOC release of 10 phylogenetically diverse marine nitrifiers. All investigated strains released DOC during growth, representing on average 5-15% of the fixed DIC. Changes in substrate concentration and temperature did not affect the proportion of fixed DIC released as DOC, but release rates varied between closely related species. Our results also indicate previous studies may have underestimated DIC fixation yields of marine nitrite oxidizers due to partial decoupling of nitrite oxidation from CO2 fixation, and due to lower observed yields in artificial compared to natural seawater medium. The results of this study provide critical values for biogeochemical models of the global carbon cycle, and help to further constrain the implications of nitrification-fueled chemoautotrophy for marine food-web functioning and the biological sequestration of carbon in the ocean.

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KW - CARBON FIXATION

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Carbon content, carbon fixation yield and dissolved organic carbon release from diverse marine nitrifiers

Abstract

Funding

UN SDGs

Austrian Fields of Science 2012

Keywords

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