Kleptoplastidic benthic foraminifera from aphotic habitats: Insights into assimilation of inorganic C, N, and S studied with sub-cellular resolution

Type Article
Date 2019-01
Language English
Author(s) Jauffrais ThierryORCID1, 2, Lekieffre Charlotte1, 3, Schweizer Magali1, Geslin Emmanuelle1, Metzger Edouard1, Bernhard Joan M.4, Jesus Bruno5, 6, Filipsson Helena L.7, Maire Olivier8, 9, Meibom Anders3, 10
Affiliation(s) 1 : Univ Angers, UMR CNRS 6112 LPG BIAF, 2 Blvd Lavoisier, F-49045 Angers 1, France.
2 : IFREMER, RBE LEAD, 101 Promenade Roger Laroque, Noumea 98897, New Caledonia.
3 : Ecole Polytech Fed Lausanne, Sch Architecture Civil & Environm Engn ENAC, Lab Biol Geochem, CH-1015 Lausanne, Switzerland.
4 : Woods Hole Oceanog Inst, Dept Geol & Geophys, Woods Hole, MA 02543 USA.
5 : Univ Nantes, Lab Mer Mol Sante, EA2160, Nantes, France.
6 : Campo Grande Univ Lisboa, Fac Sci, BioISI Biosyst & Integrat Sci Inst, Lisbon, Portugal.
7 : Lund Univ, Dept Geol, Solvegatan 12, S-22362 Lund, Sweden.
8 : Univ Bordeaux, EPOC, UMR 5805, F-33400 Talence, France.
9 : CNRS, EPOC, UMR 5805, F-33400 Talence, France.
10 : Univ Lausanne, Inst Earth Sci, Ctr Adv Surface Anal, CH-1015 Lausanne, Switzerland.
Source Environmental Microbiology (1462-2912) (Wiley), 2019-01 , Vol. 21 , N. 1 , P. 125-141
DOI 10.1111/1462-2920.14433
WOS© Times Cited 18
Abstract

The assimilation of inorganic compounds in foraminiferal metabolism compared to predation or organic matter assimilation is unknown. Here we investigate possible inorganic‐compound assimilation in Nonionellina labradorica, a common kleptoplastidic benthic foraminifer from Arctic and North Atlantic sublittoral regions. The objectives were to identify the source of the foraminiferal kleptoplasts, assess their photosynthetic functionality in light and darkness, and investigate inorganic nitrogen and sulfate assimilation. We used DNA barcoding of a ~830 bp fragment from the SSU rDNA to identify the kleptoplasts, and correlated transmission electron microscopy and nanometer‐scale secondary ion mass spectrometry (TEM‐NanoSIMS) isotopic imaging to study 13C‐bicarbonate, 15N‐ammonium, and 34S‐sulfate uptake. In addition, respiration rate measurements were determined to assess the response of N. labradorica to light. The DNA sequences established that over 80% of the kleptoplasts belonged to Thalassiosira (with 96‐99% identity), a cosmopolitan planktonic diatom. TEM‐NanoSIMS imaging revealed degraded cytoplasm and an absence of 13C assimilation in foraminifera exposed to light. Oxygen measurements showed higher respiration rates under light than dark conditions, and no O2 production was detected. These results indicate that the photosynthetic pathways in N. labradorica are not functional. Furthermore, N. labradorica assimilated both 15N‐ammonium and 34S‐sulfate into its cytoplasm, which suggests that foraminifera might have several ammonium or sulfate assimilation pathways, involving either the kleptoplasts or bona fide foraminiferal pathway(s) not yet identified.

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Jauffrais Thierry, Lekieffre Charlotte, Schweizer Magali, Geslin Emmanuelle, Metzger Edouard, Bernhard Joan M., Jesus Bruno, Filipsson Helena L., Maire Olivier, Meibom Anders (2019). Kleptoplastidic benthic foraminifera from aphotic habitats: Insights into assimilation of inorganic C, N, and S studied with sub-cellular resolution. Environmental Microbiology, 21(1), 125-141. Publisher's official version : https://doi.org/10.1111/1462-2920.14433 , Open Access version : https://archimer.ifremer.fr/doc/00460/57188/