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Kleptoplastidic benthic foraminifera from aphotic habitats: insights into assimilation of inorganic C, N and S studied with sub‐cellular resolution
Author(s) -
Jauffrais Thierry,
LeKieffre Charlotte,
Schweizer Magali,
Geslin Emmanuelle,
Metzger Edouard,
Bernhard Joan M.,
Jesus Bruno,
Filipsson Helena L.,
Maire Olivier,
Meibom Anders
Publication year - 2019
Publication title -
environmental microbiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.954
H-Index - 188
eISSN - 1462-2920
pISSN - 1462-2912
DOI - 10.1111/1462-2920.14433
Subject(s) - foraminifera , biology , benthic zone , assimilation (phonology) , photosynthesis , diatom , ammonium , nitrogen assimilation , botany , oceanography , environmental chemistry , ecology , nitrate , chemistry , philosophy , linguistics , organic chemistry , geology
Summary 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 nanometre‐scale secondary ion mass spectrometry (TEM‐NanoSIMS) isotopic imaging to study 13 C‐bicarbonate, 15 N‐ammonium and 34 S‐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 13 C assimilation in foraminifera exposed to light. Oxygen measurements showed higher respiration rates under light than dark conditions, and no O 2 production was detected. These results indicate that the photosynthetic pathways in N. labradorica are not functional. Furthermore, N. labradorica assimilated both 15 N‐ammonium and 34 S‐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.