Effect of light on photosynthetic efficiency of sequestered chloroplasts in  intertidal benthic foraminifera (&amp;lt;i&amp;gt;Haynesina germanica&amp;lt;/i&amp;gt; and &amp;lt;i&amp;gt;Ammonia tepida&amp;lt;/i&amp;gt;)

Jauffrais, Thierry; Jesus, Bruno; Metzger, Édouard; Mouget, Jean‐Luc; Jorissen, Frans; Geslin, Emmanuelle

doi:10.5194/bg-13-2715-2016

Cited by 49 publications

(70 citation statements)

References 61 publications

(83 reference statements)

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“…(1.8-2.0) indicates a primary consumer at a low irradiance (Table 2; Figure 2a). Furthermore, kleptoplast-bearing foraminifera can maintain kleptoplasts functionally for certain periods without the kleptoplast's dividing (Correia & Lee, 2002;Grzymski, Schofield, Falkowski, & Bernhard, 2002;Jauffrais et al, 2016;Lopez, 1979 Figure 2a,b).…”

Section: Effectofendobioticmicroalgaeon Foraminiferaltrophicfunctionmentioning

confidence: 99%

Compound‐specific isotope analysis of benthic foraminifer amino acids suggests microhabitat variability in rocky‐shore environments

Tsuchiya

Chikaraishi

Nomaki

et al. 2018

Ecology and Evolution

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The abundance and biomass of benthic foraminifera are high in intertidal rocky‐shore habitats. However, the availability of food to support their high biomass has been poorly studied in these habitats compared to those at seafloor covered by sediments. Previous field and laboratory observations have suggested that there is diversity in the food preferences and modes of life among rocky‐shore benthic foraminifera. In this study, we used the stable nitrogen isotopic composition of amino acids to estimate the trophic position, trophic niche, and feeding strategy of individual foraminifera species. We also characterized the configuration and structure of the endobiotic microalgae in foraminifera using transmission electron microscopy, and we identified the origin of endobionts based on nucleotide sequences. Our results demonstrated a large variation in the trophic positions of different foraminifera from the same habitat, a reflection of endobiotic features and the different modes of life and food preferences of the foraminifera. Foraminifera did not rely solely on exogenous food sources. Some species effectively used organic matter derived from endobionts in the cell cytoplasm. The high biomass and species density of benthic foraminifera found in intertidal rocky‐shore habitats are thus probably maintained by the use of multiple nitrogen resources and by microhabitat segregation among species as a consequence.

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Section: Effectofendobioticmicroalgaeon Foraminiferaltrophicfunctionmentioning

confidence: 99%

Compound‐specific isotope analysis of benthic foraminifer amino acids suggests microhabitat variability in rocky‐shore environments

Tsuchiya

Chikaraishi

Nomaki

et al. 2018

Ecology and Evolution

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“…germanica and Elphidium williamsoni had a net uptake of inorganic carbon (H 14 CO 3 ) in light, and experiments with oxygen microelectrodes demonstrated that maximal O 2 production by H . germanica depended on light intensity and light history 11 , 23 . A kleptoplastic strategy thus provides these organisms with both carbon and a source of oxygen.…”

Section: Introductionmentioning

confidence: 99%

Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer

Lekieffre

Jauffrais

Geslin

et al. 2018

Sci Rep

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Haynesina germanica, an ubiquitous benthic foraminifer in intertidal mudflats, has the remarkable ability to isolate, sequester, and use chloroplasts from microalgae. The photosynthetic functionality of these kleptoplasts has been demonstrated by measuring photosystem II quantum efficiency and O2 production rates, but the precise role of the kleptoplasts in foraminiferal metabolism is poorly understood. Thus, the mechanism and dynamics of C and N assimilation and translocation from the kleptoplasts to the foraminiferal host requires study. The objective of this study was to investigate, using correlated TEM and NanoSIMS imaging, the assimilation of inorganic C and N (here ammonium, NH4+) in individuals of a kleptoplastic benthic foraminiferal species. H. germanica specimens were incubated for 20 h in artificial seawater enriched with H13CO3− and 15NH4+ during a light/dark cycle. All specimens (n = 12) incorporated 13C into their endoplasm stored primarily in the form of lipid droplets. A control incubation in darkness resulted in no 13C-uptake, strongly suggesting that photosynthesis is the process dominating inorganic C assimilation. Ammonium assimilation was observed both with and without light, with diffuse 15N-enrichment throughout the cytoplasm and distinct 15N-hotspots in fibrillar vesicles, electron-opaque bodies, tubulin paracrystals, bacterial associates, and, rarely and at moderate levels, in kleptoplasts. The latter observation might indicate that the kleptoplasts are involved in N assimilation. However, the higher N assimilation observed in the foraminiferal endoplasm incubated without light suggests that another cytoplasmic pathway is dominant, at least in darkness. This study clearly shows the advantage provided by the kleptoplasts as an additional source of carbon and provides observations of ammonium uptake by the foraminiferal cell.

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“…(d) Diversity of gene products from communities of eukaryotic excavate symbionts in termite guts reflects the environment of their host communities (Duarte, Nobre, Borges, & Nunes, 2018); (e) Hermatypic coral are dependent on the dinoflagellate Symbiodinium for 95% of their energy (Gilbert et al, 2010). (f) Acanthamoebae host amoeba-resistant bacteria like Legionella pneumophila, which have evolved to resist digestion and in some cases even to survive within human macrophages (Greub & Raoult, 2004;Loret & Greub, 2010); (g) Ciliate Paramecium tetraurelia hosts bacteria Caedibacter taeniospiralis in its cytoplasm that can kill non-host P. tetraurelia and protect current hosts from its killer mechanism (Grosser et al, 2018); (h) Single-cellular foraminifera can "steal" chloroplasts from the diatoms and other algae they eat to use for photosynthesis-a phenomenon known as kleptoplasty (Clark et al, 1990;Jauffrais et al, 2016); (i) the parasitic wasp Asobara tabida needs Wolbachia bacteria to develop into adulthood and form its ovaries properly (Gilbert et al, 2010). (j) Acrythosiphon pisum, otherwise known as pea aphids, need gene products from the endosymbiotic bacterium Buchnera aphidicola to make essential amino acids it does not get from its diet of sap (Wilson et al, 2010) bacteria in pea aphids gained a gene cluster from another endosymbiont, Cardinium or Rickettsia, through lateral gene transfer (Nikoh et al, 2014).…”

Section: Hologenomes: a Spectrum Of Intimacymentioning

confidence: 99%

“…Host ( (2011) Amoebozoa Acanthamoeaba Diverse bacteria Greub and Raoult, (2004) and Loret and Greub, (2010) Neoparamoeba sp Perkinsela sp. (Excavata) Nowak and Archibald (2018) Rhizaria Foraminifera Dinoflagellates, diatoms Jauffrais et al (2016) and Pillet et al (2011) Alveolata Paramecium tetraurelia Caedibacter taeniospiralis Grosser et al (2018)…”

Section: Host Cladementioning

confidence: 99%

The concept of the hologenome, an epigenetic phenomenon, challenges aspects of the modern evolutionary synthesis

2019

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John Tyler Bonner's call to re‐evaluate evolutionary theory in light of major transitions in life on Earth (e.g., from the first origins of microbial life to the evolution of sex, and the origins of multicellularity) resonate with recent discoveries on epigenetics and the concept of the hologenome. Current studies of genome evolution often mistakenly focus only on the inheritance of DNA between parent and offspring. These are in line with the widely accepted Neo‐Darwinian framework that pairs Mendelian genetics with an emphasis on natural selection as explanations for the evolution of biodiversity on Earth. Increasing evidence for widespread symbioses complicates this narrative, as is seen in Scott Gilbert's discussion of the concept of the holobiont in this series: Organisms across the tree of life coexist with substantial influence on one another through endosymbiosis, symbioses, and host‐associated microbiomes. The holobiont theory, coupled with observations from molecular studies, also requires us to understand genomes in a new way—by considering the interactions underlain by the genome of a host plus its associated microbes, a conglomerate entity referred to as the hologenome. We argue that the complex patterns of inheritance of these genomes coupled with the influence of symbionts on host gene expression make the concept of the hologenome an epigenetic phenomenon. We further argue that the aspects of the hologenome challenge of the modern evolutionary synthesis, which requires updating to remain consistent with Darwin's intent of providing natural laws that underlie the evolution of life on Earth.

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Effect of light on photosynthetic efficiency of sequestered chloroplasts in intertidal benthic foraminifera (<i>Haynesina germanica</i> and <i>Ammonia tepida</i>)

Cited by 49 publications

References 61 publications

Compound‐specific isotope analysis of benthic foraminifer amino acids suggests microhabitat variability in rocky‐shore environments

Compound‐specific isotope analysis of benthic foraminifer amino acids suggests microhabitat variability in rocky‐shore environments

Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer

The concept of the hologenome, an epigenetic phenomenon, challenges aspects of the modern evolutionary synthesis

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