Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments

Gomaa, Fatma; Utter, Daniel R.; Powers, Christopher; Beaudoin, David J.; Edgcomb, Virginia P.; Filipsson, Helena L.; Hansel, Colleen M.; Wankel, Scott D.; Zhang, Ying; Bernhard, Joan M.

doi:10.1126/sciadv.abf1586

Cited by 36 publications

(76 citation statements)

References 78 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This indicates benthic foraminiferal metabolism is not uniform across species. While the ability to perform denitrification and anaerobic energy metabolism are established for N. stella (4,23), we show here that N. stella of the SBB are adept at surviving anoxia, having metabolically flexible mitochondria that function in coordination with the predicted metabolism of its peroxisomes. The metabolism predicted for B. argentea suggested the capacity to digest food vacuole contents as a facultative anaerobe.…”

Section: Discussionmentioning

confidence: 65%

“…N. stella sequesters chloroplasts (23,29,30), likely from prey, proliferates peroxisomeendoplasmic reticulum (P-ER) complexes (7), and apparently lacks food vacuoles (23). In contrast, B. argentea is abundant at the basin's flanks, rarely occurring in the most oxygendepleted conditions (9), contains solitary to small groups of peroxisomes, and exhibits evidence of digestion of chloroplasts and other organics (5).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Powers

Gomaa

Billings

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

Certain benthic foraminifera are known to thrive in marine sediments with low oxygen or even without detectable oxygen. Potential survival avenues used by these supposedly aerobic protists include fermentation and anaerobic respiration, although details on their adaptive mechanisms remain somewhat elusive. To better understand the metabolic versatility of foraminifera, we studied two benthic species that thrive in oxygen-depleted marine sediments. Here we detail, via transcriptomics and metatranscriptomics, differential gene expression of Nonionella stella and Bolivina argentea, collected from Santa Barbara Basin, California, USA, in response to varied oxygenation and chemical amendments. Organelle-specific metabolic reconstructions revealed that these two species utilize adaptable mitochondrial and peroxisomal metabolism that reflect their differing lifestyles. N. stella, most abundant in anoxia and characterized by the lack of food vacuoles and the abundance of intracellular lipid droplets, was predicted to couple the putative peroxisomal beta-oxidation and glyoxylate cycle with a versatile electron transport system and a partial TCA cycle running in the reductive direction. In contrast, B. argentea, most abundant in hypoxia and contains food vacuoles, was predicted to utilize the putative peroxisomal gluconeogenesis and a full TCA cycle but lacks the expression of key beta-oxidation and glyoxylate cycle genes. These metabolic adaptations likely confer ecological success while encountering deoxygenation and illuminate the importance of metabolic modifications and interactions between mitochondria and peroxisomes in protists.ImportanceForaminiferan protists are nearly ubiquitous in today’s oceans and likely were major components of the Neoproterozoic protistan community. While largely considered aerobic, certain foraminifera demonstrate surprising adaptability to hypoxia and anoxia, contributing to biogeochemical cycling in benthic environments. The analyses of Rhizarian adaptive metabolism set the stage for studying other microeukaryotes under increasing ocean deoxygenation. Revealing the metabolic roles of foraminifera in anaerobic biogeochemical cycling should spur reassessments of existing paleoecological datasets as well as new perspectives on the metabolic evolution of eukaryotic cells.

show abstract

Section: Discussionmentioning

confidence: 65%

Section: Introductionmentioning

confidence: 99%

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Powers

Gomaa

Billings

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…In addition, the Globobulimina genome contains a diverse gene family encoding for nitrate transporters (Nrt) (11), a finding that is consistent with the accumulation of an intracellular NO 3- storage in denitrifying rotaliids (8-10, 16). More recent studies reported the presence of those genes in at least two additional species of foraminifera and provide alternative suggestions on the nitrate reductase homolog missing from the earlier model of denitrification in foraminifera (17, 18). The rotaliids ability to respire both oxygen (O 2 ) and NO 3- marks them as facultative anaerobes that are able to thrive in both aerobic and anaerobic conditions.…”

Section: Introductionmentioning

confidence: 81%

Denitrification in foraminifera has ancient origin and is complemented by associated bacteria

Woehle

Roy

Glock

et al. 2021

Preprint

View full text Add to dashboard Cite

Benthic foraminifera are unicellular eukaryotes that inhabit sediments of aquatic environments. Several foraminifera of the order Rotaliida are known to store and use nitrate for denitrification, a unique energy metabolism among eukaryotes. The rotaliid Globobulimina spp. has been shown to encode an incomplete denitrification pathway of bacterial origins. However, the prevalence of denitrification genes in foraminifera remains unknown and the missing denitrification pathway components are elusive. Analysing transcriptomes and metagenomes of ten foraminifera species from the Peruvian oxygen minimum zone, we show that denitrification genes are highly conserved in foraminifera. We infer of the last common ancestor of denitrifying foraminifera, which enables us to predict further denitrifying species. Additionally, an examination of the foraminifera microbiota reveals evidence for a stable interaction with Desulfobacteracea, which harbour genes that complement the foraminifera denitrification pathway. Our results provide evidence that foraminiferal denitrification is complemented by the foraminifera microbiome. The interaction of Foraminifera with their resident bacteria is at the basis of foraminifera adaptation to anaerobic environments that manifested in ecological success within oxygen depleted habitats.

show abstract

“…It has also been suggested that foraminifera may sometimes be transported into seeps and can also occur at tze SMTZ, but they likely not live in those sediment layers permanently (Bernhard and Bowser, 1999). Foraminfiera in general have several metabolic strategies to cope with anoxic environments (Gomaa et al, 2021) of which many remain to be understudied.…”

Section: Association With Putative Methanotrophsmentioning

confidence: 99%

Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy

Schmidt

Geslin²,

Bernhard

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Abstract. Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material along with entrained bacteria). However, the role of such foraminifera in the benthic food-web remains understudied. As foraminifera may associate with methanotrophic bacteria, which are 13C-depleted, feeding on them has been suggested to cause negative δ13C values in the foraminiferal cytoplasm and/or calcite. To test whether the foraminiferal diet includes methanotrophs, we performed a short-term (1 d) feeding experiment with Nonionellina labradorica from an active Arctic methane-emission site (Storfjordrenna, Barents Sea) using the marine methanotroph Methyloprofundus sedimenti, and analyzed N. labradorica cytology via Transmission Electron microscopy (TEM). We hypothesized that M. sedimenti would be visible, as evidenced by their ultrastructure, in degradation vacuoles after this feeding experiment. Sediment grains (mostly clay) occurred inside one or several degradation vacuoles in all foraminifers. In 24 % of the specimens from the feeding experiment degradation vacuoles also contained bacteria, although none could be confirmed to be the offered M. sedimenti. Observations of the area adjacent to the aperture after 20 h incubation revealed three putative methanotrophs, close to clay particles. These methanotrophs were identified based on internal characteristics such as a type I stacked intracytoplasmic membranes (ICM), storage granules (SG) and gram-negative cell walls (GNCW). Furthermore, N. labradorica specimens were examined for specific adaptations to this active Arctic methane-emission site; we noted the absence of bacterial endobionts in all specimens examined but confirmed the presence of kleptoplasts, which were often partially degraded. Based on these observations, we suggest that M. sedimenti can be consumed by N. labradorica via untargeted grazing in seeps and that N. labradorica can be generally classified as a deposit feeder at this Arctic site. These results suggest that if methanothrophs are available to the foraminifera in their habitat, their non-selective uptake could make a substantial contribution to altering δ13Ctest values. This in turn may impact metazoans grazing on benthic foraminifera by altering their δ13C signature.

show abstract

Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments

Cited by 36 publications

References 78 publications

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Denitrification in foraminifera has ancient origin and is complemented by associated bacteria

Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy

Contact Info

Product

Resources

About