Denitrification likely catalyzed by endobionts in an allogromiid foraminifer

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 N 2 (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.

Uptake of phytodetritus by benthic foraminifera under oxygen depletion at the Indian margin (Arabian Sea)

“…This surprising ability to accumulate nitrate and its respiration to dinitrogen gas was later confirmed in benthic foraminifera in OMZ sediments off the Chilean coast (Hogslund et al, 2008) and demonstrated in laboratory experiments (Pina-Ochoa et al, 2010). However, in at least one species, symbiotic bacteria appear to be responsible for respiring the nitrate, not the foraminifera (Bernhard et al, 2012). Since most other eukaryotic organisms, especially macrofauna, are not as tolerant to hypoxia as foraminifera (Josefson and Widbom, 1988), they often are absent from sediments in the core of the OMZ ).…”

Insights into foraminiferal influences on microfabrics of microbialites at Highborne Cay, Bahamas

“…2 and 3). If deeply infaunal foraminifera do not migrate, they likely rely on anaerobic metabolism, such as denitrification, which is documented in a considerable variety of foraminifera and/or their symbionts (25,26). It is not known at this time if any of the Highborne Cay microbialite foraminifera perform complete denitrification.…”

Changes in ultrastructural features of the foraminifera Ammonia spp. in response to anoxic conditions: Field and laboratory observations

“…(phylotype 6 and phylotype unknown) may be a host to various species of intracellular bacteria, and that the bacterial assemblages comprising the foraminiferal microbiome may change in time and space. Various endobionts have been described for other foraminiferal species that inhabit anoxic sediments (e.g., Bernhard, 2003;Bernhard et al, 2012;Tsuchiya et al, 2015;Bernhard et al, 2017). Therefore, the presence of bacterial endobionts in foraminifera coming from anoxic sediments seems relatively widespread.…”

“…Anaerobic metabolism, namely denitrification via an intracellular nitrate pool, has been demonstrated for various species of benthic foraminifera (Risgaard-Petersen et al, 2006;Piña-Ochoa et al, 2010;Bernhard et al, 2012). However, it is currently not known whether denitrification is catalyzed by the foraminifera proper, or by potential endosymbionts of the foraminifera; evidence for both strategies exists (Risgaard-Petersen et al, 2006;Bernhard et al, 2012).…”

“…Presence of potential endosymbionts involved in denitrification or other biogeochemical functions, enabling foraminifera to survive anoxia, can be detected and visualized. Many species of benthic foraminifera, which inhabit low-oxygen environments, seem to possess various potential endosymbionts (e.g., Bernhard, 1993;Bernhard, 1996;Bernhard, 2003;Bernhard et al, 2012;Tsuchiya et al, 2015;Bernhard et al, 2017). Extensive peroxisomes complexed with endoplasmic reticulum, which are atypical in foraminifera from aerated habitats, have also been linked to foraminiferal survival in low-oxygen and chemocline sediments (e.g., Nyholm and Nyholm 1975, Bernhard, 1996, Bernhard and Bowser, 2008.…”