Abstract
Nitrogen can be a limiting macronutrient for carbon uptake by the marine biosphere. The process of denitrification (conversion of nitrate to gaseous compounds, including N2 (nitrogen gas)) removes bioavailable nitrogen, particularly in marine sediments, making it a key factor in the marine nitrogen budget. Benthic foraminifera reportedly perform complete denitrification, a process previously considered nearly exclusively performed by bacteria and archaea. If the ability to denitrify is widespread among these diverse and abundant protists, a paradigm shift is required for biogeochemistry and marine microbial ecology. However, to date, the mechanisms of foraminiferal denitrification are unclear, and it is possible that the ability to perform complete denitrification is because of the symbiont metabolism in some foraminiferal species. Using sequence analysis and GeneFISH, we show that for a symbiont-bearing foraminifer, the potential for denitrification resides in the endobionts. Results also identify the endobionts as denitrifying pseudomonads and show that the allogromiid accumulates nitrate intracellularly, presumably for use in denitrification. Endobionts have been observed within many foraminiferal species, and in the case of associations with denitrifying bacteria, may provide fitness for survival in anoxic conditions. These associations may have been a driving force for early foraminiferal diversification, which is thought to have occurred in the Neoproterozoic era when anoxia was widespread.
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Acknowledgements
We thank the captain and crew of the RV Robert Gordon Sproul, all science party members for their help with sampling, Joe DeGiorgis for early attempts to identify vacuole contents, Sam Bowser and Amanda Andreas for assistance with elemental mapping, Edward Leadbetter for insights on bacterial metabolism and three anonymous reviewers for helpful comments on an earlier manuscript version. This research was supported by NSF Grant EF-0702491 to JMB, KLC and VPE; some ship support was provided by NSF Grant MCB-0604084 to VPE and JMB.
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Bernhard, J., Edgcomb, V., Casciotti, K. et al. Denitrification likely catalyzed by endobionts in an allogromiid foraminifer. ISME J 6, 951–960 (2012). https://doi.org/10.1038/ismej.2011.171
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DOI: https://doi.org/10.1038/ismej.2011.171
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