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

Abstract

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 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.

Response of a kleptoplastidic foraminifer to heterotrophic starvation: photosynthesis and lipid droplet biogenesis

“…Nevertheless, diatom nuclear DNA was amplified in the present and other studies (Jauffrais et al, 2019), which supports the hypothesis that the diatom nucleus may be ingested, kept for some time (as the DNA can still be amplified) and then digested in kleptoplastidic foraminiferal species (within a few days?) as in other kleptoplastidic organisms (Green et al, 2000, Nagai et al, 2008, Hansen et al, 2016.…”

“…the pyrenoid, girdle lamella, thylakoids, the four membranes around the kleptoplasts, the absence of starch accumulation-and the molecular analyses show that E. williamsoni ingests mainly diatom kleptoplasts. Previous studies on coastal (Knight & Mantoura, 1985, Goldstein et al, 2004, Pillet et al, 2011, Goldstein & Richardson, 2018 and deep-sea kleptoplastidic foraminifera (Bernhard & Bowser, 1999, Grzymski et al, 2002, Jauffrais et al, 2019 show the same preference for diatoms. A closer examination done using the 18S rDNA sequences compared to diatom 18S sequences available from GenBank indicates that all identified diatoms were mostly relatively large epipelic genera living in intertidal mudflats along the European Atlantic coast (Ribeiro et al, 2003, Meleder et al, 2007, Jesus et al, 2009.…”

“…Re021-16S, Re021-18S, Re024-16S, Re024-18S) were sequenced. PCR amplification and cloning steps are described in detail in Jauffrais et al (2019).…”

“…Foraminiferal kleptoplast functions and characteristics are still poorly understood and therefore their role in biogeochemical cycles and in the foraminiferal metabolism needs clarifications (Jauffrais et al, 2019, LeKieffre et al, 2018b. Previous research has shown that these kleptoplasts originate from microalgae, essentially diatoms (Pillet et al, 2011).…”

Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts

“…In this regard, δ 13 C values measured on different amino acids from the symbiotic species Orbulina universa are consistent with two isotopically distinct sources of carbon and nitrogen, isotopically heavy metabolic carbon and nitrogen from its symbionts and relatively lighter carbon and nitrogen from the diet [6,7]. It is also likely that planktonic foraminifer can assimilate inorganic nitrogen from seawater if it is available [2,5,8] because ammonium assimilation has already been reported in a benthic species with inactive kleptoplasts [9].…”