Molecular Identification of Sequestered Diatom Chloroplasts and Kleptoplastidy in Foraminifera

Pillet, Loïc; Vargas, Colomban de; Pawłowski, Jan

doi:10.1016/j.protis.2010.10.001

Cited by 85 publications

(94 citation statements)

References 37 publications

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“…mainly from diatoms (Lopez, 1979;Knight and Mantoura, 1985;Grzymski et al, 2002;Goldstein, 2004). This was confirmed by experimental feeding studies (Correia and Lee, 2002a;Austin et al, 2005) and by molecular analysis of kleptoplastic foraminifera from different environments (Pillet et al, 2011;Tsuchiya et al, 2015). Foraminifera from intertidal mudflat environments (e.g.…”

Section: T Jauffrais Et Al: Effect Of Light On Photosynthetic Efficmentioning

confidence: 61%

“…Kleptoplastic foraminifera are found in intertidal sediments (e.g. Haynesina, Elphidium and Xiphophaga) (Lopez, 1979;Lee, 2000, 2002a, b;Goldstein et al, 2010;Pillet et al, 2011), low oxygenated aphotic environments (Nonionella, Nonionellina, Stainforthia) (Bernhard and Bowser, 1999;Grzymski et al, 2002) and shallow-water sediments (Bulimina elegantissima) (Bernhard and Bowser, 1999). The role of chloroplasts sequestered by benthic foraminifera is poorly known and photosynthetic functions have only been studied in a few mudflat species (Elphidium williamsoni, Elphidium excavatum and Haynesina germanica) (Lopez, 1979;Lee, 2000, 2002a, b;F.…”

Section: T Jauffrais Et Al: Effect Of Light On Photosynthetic Efficmentioning

confidence: 99%

“…Foraminifera from intertidal mudflat environments (e.g. H. germanica, A. tepida) feed mostly on pennate diatoms (Pillet et al, 2011) which are the dominant microalgae in intertidal mudflat sediments (MacIntyre et al, 1996;Jesus et al, 2009). Furthermore, in these transitional coastal environments (e.g.…”

Section: T Jauffrais Et Al: Effect Of Light On Photosynthetic Efficmentioning

confidence: 99%

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

et al. 2016

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Abstract. Some benthic foraminifera have the ability to incorporate functional chloroplasts from diatoms (kleptoplasty). Our objective was to investigate chloroplast functionality of two benthic foraminifera (Haynesina germanica and Ammonia tepida) exposed to different irradiance levels (0, 25, 70 µmol photon m −2 s −1 ) using spectral reflectance, epifluorescence observations, oxygen evolution and pulse amplitude modulated (PAM) fluorometry (maximum photosystem II quantum efficiency (Fv/Fm) and rapid light curves (RLC)). Our results clearly showed that H. germanica was capable of using its kleptoplasts for more than 1 week while A. tepida showed very limited kleptoplastic ability with maximum photosystem II quantum efficiency (Fv/Fm = 0.4), much lower than H. germanica and decreasing to zero in only 1 day. Only H. germanica showed net oxygen production with a compensation point at 24 µmol photon m −2 s −1 and a production up to 1000 pmol O 2 cell −1 day −1 at 300 µmol photon m −2 s −1 . Haynesina germanica Fv/Fm slowly decreased from 0.65 to 0.55 in 7 days when kept in darkness; however, it quickly decreased to 0.2 under high light. Kleptoplast functional time was thus estimated between 11 and 21 days in darkness and between 7 and 8 days at high light. These results emphasize that studies about foraminifera kleptoplasty must take into account light history. Additionally, this study showed that the kleptoplasts are unlikely to be completely functional, thus requiring continuous chloroplast resupply from foraminifera food source. The advantages of keeping functional chloroplasts are discussed but more information is needed to better understand foraminifera feeding strategies.

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Section: T Jauffrais Et Al: Effect Of Light On Photosynthetic Efficmentioning

confidence: 61%

Section: T Jauffrais Et Al: Effect Of Light On Photosynthetic Efficmentioning

confidence: 99%

Section: T Jauffrais Et Al: Effect Of Light On Photosynthetic Efficmentioning

confidence: 99%

See 1 more Smart Citation

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

et al. 2016

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“…Firstly, the structure of the pyrenoid (one transecting lamella surrounded by one membrane), the presence of a girdle lamella and, thylakoids, and the absence of starch accumulation, together other evidence (ultrastructural, pigment and molecular analyses of the sequestered plastids, Goldstein et al, 2004;Knight and Mantoura, 1985;Pillet et al, 2011, Jauffrais et al 2016, suggest that the kleptoplasts in all seven species belonged to diatoms. Similar ultrastructural, pigment and molecular analyses confirm a similar source for deep-water kleptoplastic benthic foraminifera (Bernhard and Bowser 1999;Grzymski et al, 2001).…”

Section: Discussionmentioning

confidence: 97%

“…These foraminiferal species mainly ingest diatoms (Knight and Mantoura, 1985;Bowser 1999, Goldstein et al, 2004;Pillet et al, 2011;Tsuchiya et al, 2015;Jauffrais et al, 2017) but have different strategies for feeding and sequestration (Lopez, 1979;Grzymski et al, 2002;Austin et al, 2005;Jauffrais et al, 2016b). In some foraminiferal species, the kleptoplasts are degraded within hours, possibly as a result of a digestive process, while in other species they are kept and/or remain functional for weeks to months (Lopez, 1979;Lee et al, 1988;Cedhagen, 1991;Lee, 2000, 2002a, b;Grzymski et al, 2002;Tsuchiya et al, 2015;Jauffrais et al, 2016b).…”

Section: Introductionmentioning

confidence: 99%

Ultrastructure and distribution of kleptoplasts in benthic foraminifera from shallow-water (photic) habitats

Jauffrais

Lekieffre

Koho

et al. 2018

Marine Micropaleontology

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Assimilation, sequestration and maintenance of foreign chloroplasts inside an organism is termed "chloroplast sequestration" or "kleptoplasty". This phenomenon is known in certain benthic foraminifera, in which such kleptoplasts can be found both intact and functional, but with different retention times depending on foraminiferal species. In the present study, seven species of benthic foraminifera (Haynesina germanica, Elphidium williamsoni, E. selseyense, E. oceanense, E. aff. E. crispum, Planoglabratella opercularis and Ammonia sp.) were collected from shallow-water benthic habitats and examined with transmission electron microscope (TEM) for cellular ultrastructure to ascertain attributes of kleptoplasts. Results indicate that all these foraminiferal taxa actively obtain kleptoplasts but organized them differently within their endoplasm. In some species, the kleptoplasts were evenly distributed throughout the endoplasm (e.g., H. germanica, E. oceanense, Ammonia sp.), whereas other species consistently had plastids distributed close to the external cell membrane (e.g., Elphidium williamsoni, E. selseyense, P. opercularis).Chloroplast degradation also seemed to differ between species, as many degraded plastids were found in Ammonia sp. and E. oceanense compared to other investigated species. Digestion ability, along with different feeding and sequestration strategies may explain the differences in retention time between taxa. Additionally, the organization of the sequestered plastids within the endoplasm may also suggest behavioral strategies to expose and/or protect the sequestered plastids to/from light and/or to favor gas and/or nutrient exchange with their surrounding habitats.

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Trophic strategies of intertidal foraminifera explored with single‐cell microbiome metabarcoding and morphological methods: What is on the menu?

Schweizer

Jauffrais

Choquel

et al. 2022

Ecology and Evolution

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In mudflats, interactions and transfers of nutrients and secondary metabolites may drive ecosystems and biodiversity. Foraminifera have complex trophic strategies as they often rely on bacteria and eukaryotes or on potential symbionts for carbon and nitrogen resources. The capacity of these protists to use a wide range of adaptive mechanisms requires clarifying the relationships between them and their microbial associates. Here, we investigate the interactions of three foraminiferal species with nearby organisms in situ, by coupling molecular (cloning/Sanger and high‐throughput sequencing) and direct counting and morphological identification with microscopy. This coupling allows the identification of the organisms found in or around three foraminiferal species through molecular tools combined with a direct counting of foraminifera and diatoms present in situ through microscopy methods. Depending on foraminiferal species, and in addition to diatom biomass, diatom frustule shape, size and species are key factors driving the abundance and diversity of foraminifera in mudflat habitats. Three different trophic strategies were deduced for the foraminifera investigated in this study: Ammonia sp. T6 has an opportunistic strategy and is feeding on bacteria, nematoda, fungi, and diatoms when abundant; Elphidium oceanense is feeding mainly on diatoms, mixed with other preys when they are less abundant; and Haynesina germanica is feeding almost solely on medium‐large pennate diatoms. Although there are limitations due to the lack of species coverage in DNA sequence databases and to the difficulty to compare morphological and molecular data, this study highlights the relevance of combining molecular with morphological tools to study trophic interactions and microbiome communities of protists at the single‐cell scale.

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Molecular Identification of Sequestered Diatom Chloroplasts and Kleptoplastidy in Foraminifera

Cited by 85 publications

References 37 publications

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

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

Ultrastructure and distribution of kleptoplasts in benthic foraminifera from shallow-water (photic) habitats

Trophic strategies of intertidal foraminifera explored with single‐cell microbiome metabarcoding and morphological methods: What is on the menu?

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Molecular Identification of Sequestered Diatom Chloroplasts and Kleptoplastidy in Foraminifera

Cited by 85 publications

References 37 publications

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

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

Ultrastructure and distribution of kleptoplasts in benthic foraminifera from shallow-water (photic) habitats

Trophic strategies of intertidal foraminifera explored with single‐cell microbiome metabarcoding and morphological methods: What is on the menu?

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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>)

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