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Article ; Online: Continuous reproduction of planktonic foraminifera in laboratory culture.

Meilland, Julie / Siccha, Michael / Morard, Raphaël / Kucera, Michal

2024 Volume 71, Issue 3, Page(s) e13022

Abstract: Planktonic foraminifera were long considered obligate sexual outbreeders but recent observations have shown that nonspinose species can reproduce by multiple fission. The frequency of multiple fission appears low but the survival rate of the offspring is ...

Abstract	Planktonic foraminifera were long considered obligate sexual outbreeders but recent observations have shown that nonspinose species can reproduce by multiple fission. The frequency of multiple fission appears low but the survival rate of the offspring is high and specimens approaching fission can be distinguished. We made use of this observation and established a culturing protocol aimed at enhancing the detection and frequency of fission. Using this protocol, we selectively cultured specimens of Neogloboquadrina pachyderma and raised the frequency of reproduction by fission in culture from 3% in randomly selected specimens to almost 60%. By feeding the resulting offspring different strains of live diatoms, we obtained a thriving offspring population and during the subsequent 6 months of culturing, we observed two more successive generations produced by fission. This provides evidence that in nonspinose species of planktonic foraminifera, reproduction by multiple fission is likely clonal and corresponds to the schizont phase known from benthic foraminifera. We subsequently tested if a similar culturing strategy could be applied to Globigerinita glutinata, representing a different clade of planktonic foraminifera, and we were indeed able to obtain offspring via multiple fission in this species. This work opens new avenues for laboratory-based experimental work with planktonic foraminifera.
MeSH term(s)	Foraminifera/physiology ; Reproduction ; Plankton ; Diatoms/growth & development ; Diatoms/physiology
Language	English
Publishing date	2024-02-25
Publishing country	United States
Document type	Journal Article
ZDB-ID	1147218-2
ISSN	1550-7408 ; 1066-5234
ISSN (online)	1550-7408
ISSN	1066-5234
DOI	10.1111/jeu.13022
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Article ; Online: Macroevolutionary patterns in intragenomic rDNA variability among planktonic foraminifera.

Greco, Mattia / Morard, Raphaël / Darling, Kate / Kucera, Michal

PeerJ

2023 Volume 11, Page(s) e15255

Abstract: Ribosomal intragenomic variability in prokaryotes and eukaryotes is a genomic feature commonly studied for its inflationary impact on molecular diversity assessments. However, the evolutionary mechanisms and distribution of this phenomenon within a ... ...

Abstract	Ribosomal intragenomic variability in prokaryotes and eukaryotes is a genomic feature commonly studied for its inflationary impact on molecular diversity assessments. However, the evolutionary mechanisms and distribution of this phenomenon within a microbial group are rarely explored. Here, we investigate the intragenomic variability in 33 species of planktonic foraminifera, calcifying marine protists, by inspecting 2,403 partial SSU sequences obtained from single-cell clone libraries. Our analyses show that polymorphisms are common among planktonic foraminifera species, but the number of polymorphic sites significantly differs among clades. With our molecular simulations, we could assess that most of these mutations are located in paired regions that do not affect the secondary structure of the SSU fragment. Finally, by mapping the number of polymorphic sites on the phylogeny of the clades, we were able to discuss the evolution and potential sources of intragenomic variability in planktonic foraminifera, linking this trait to the distinctive nuclear and genomic dynamics of this microbial group.
MeSH term(s)	Foraminifera/genetics ; DNA, Ribosomal/chemistry ; Plankton/genetics ; Phylogeny ; Eukaryota/genetics
Chemical Substances	DNA, Ribosomal
Language	English
Publishing date	2023-04-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2703241-3
ISSN	2167-8359 ; 2167-8359
ISSN (online)	2167-8359
ISSN	2167-8359
DOI	10.7717/peerj.15255
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Book ; Online: Deep Visual-Genetic Biometrics for Taxonomic Classification of Rare Species

Karaderi, Tayfun / Burghardt, Tilo / Morard, Raphael / Schmidt, Daniela

2023

Abstract: Visual as well as genetic biometrics are routinely employed to identify species and individuals in biological applications. However, no attempts have been made in this domain to computationally enhance visual classification of rare classes with little ... ...

Abstract	Visual as well as genetic biometrics are routinely employed to identify species and individuals in biological applications. However, no attempts have been made in this domain to computationally enhance visual classification of rare classes with little image data via genetics. In this paper, we thus propose aligned visual-genetic inference spaces with the aim to implicitly encode cross-domain associations for improved performance. We demonstrate for the first time that such alignment can be achieved via deep embedding models and that the approach is directly applicable to boosting long-tailed recognition (LTR) particularly for rare species. We experimentally demonstrate the efficacy of the concept via application to microscopic imagery of 30k+ planktic foraminifer shells across 32 species when used together with independent genetic data samples. Most importantly for practitioners, we show that visual-genetic alignment can significantly benefit visual-only recognition of the rarest species. Technically, we pre-train a visual ResNet50 deep learning model using triplet loss formulations to create an initial embedding space. We re-structure this space based on genetic anchors embedded via a Sequence Graph Transform (SGT) and linked to visual data by cross-domain cosine alignment. We show that an LTR approach improves the state-of-the-art across all benchmarks and that adding our visual-genetic alignment improves per-class and particularly rare tail class benchmarks significantly further. We conclude that visual-genetic alignment can be a highly effective tool for complementing visual biological data containing rare classes. The concept proposed may serve as an important future tool for integrating genetics and imageomics towards a more complete scientific representation of taxonomic spaces and life itself. Code, weights, and data splits are published for full reproducibility.
Keywords	Computer Science - Computer Vision and Pattern Recognition ; Computer Science - Artificial Intelligence ; Computer Science - Machine Learning ; Quantitative Biology - Quantitative Methods
Subject code	004
Publishing date	2023-05-11
Publishing country	us
Document type	Book ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Collection of X-ray micro computed tomography images of shells of planktic foraminifera with curated taxonomy.

Siccha, Michael / Morard, Raphaël / Meilland, Julie / Iwasaki, Shinya / Kucera, Michal / Kimoto, Katsunori

Scientific data

2023 Volume 10, Issue 1, Page(s) 679

Abstract: Calcite shells of planktic foraminifera (Protista, Rhizaria) constitute a large portion of deep-sea sediments. The shells are constructed by sequential addition of partly overlapping chambers with diverse shapes, resulting in complex shell architectures, ...

Abstract	Calcite shells of planktic foraminifera (Protista, Rhizaria) constitute a large portion of deep-sea sediments. The shells are constructed by sequential addition of partly overlapping chambers with diverse shapes, resulting in complex shell architectures, which are genetically fixed and diagnostic at the species level. The characterisation of the complete architecture requires three-dimensional imaging of the shell, including the partially or entirely covered juvenile chambers. Here we provide reconstructed x-ray micro computed tomography image stacks of 179 specimens of extant planktic foraminifera collected from plankton tows, sediment traps and surface sediments. The specimens have fully resolved and curated taxonomy and represent 43 of the currently recognised 48 holoplanktic species and subspecies. The image stacks form a basis for further applications, such as the characterisation of the architectural morphospace of the extant taxa, allowing studies of species functional ecology, calcification intensity and reconstructions of phylogenetic relationships.
MeSH term(s)	Ecology ; Foraminifera ; Phylogeny ; X-Ray Microtomography
Language	English
Publishing date	2023-10-05
Publishing country	England
Document type	Dataset ; Journal Article
ZDB-ID	2775191-0
ISSN	2052-4463 ; 2052-4463
ISSN (online)	2052-4463
ISSN	2052-4463
DOI	10.1038/s41597-023-02498-0
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Article ; Online: Shared ancestry of algal symbiosis and chloroplast sequestration in foraminifera.

Pinko, Doron / Abramovich, Sigal / Rahav, Eyal / Belkin, Natalia / Rubin-Blum, Maxim / Kucera, Michal / Morard, Raphaël / Holzmann, Maria / Abdu, Uri

Science advances

2023 Volume 9, Issue 41, Page(s) eadi3401

Abstract: Foraminifera are unicellular organisms that established the most diverse algal symbioses in the marine realm. Endosymbiosis repeatedly evolved in several lineages, while some engaged in the sequestration of chloroplasts, known as kleptoplasty. So far, ... ...

Abstract	Foraminifera are unicellular organisms that established the most diverse algal symbioses in the marine realm. Endosymbiosis repeatedly evolved in several lineages, while some engaged in the sequestration of chloroplasts, known as kleptoplasty. So far, kleptoplasty has been documented exclusively in the rotaliid clade. Here, we report the discovery of kleptoplasty in the species
MeSH term(s)	Phylogeny ; Symbiosis/genetics ; Foraminifera/genetics ; Chloroplasts/genetics
Language	English
Publishing date	2023-10-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	2810933-8
ISSN	2375-2548 ; 2375-2548
ISSN (online)	2375-2548
ISSN	2375-2548
DOI	10.1126/sciadv.adi3401
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Article ; Online: Invasion success of a Lessepsian symbiont-bearing foraminifera linked to high dispersal ability, preadaptation and suppression of sexual reproduction.

S Raposo, Débora / A Zufall, Rebecca / Caruso, Antonio / Titelboim, Danna / Abramovich, Sigal / Hassenrück, Christiane / Kucera, Michal / Morard, Raphaël

Scientific reports

2023 Volume 13, Issue 1, Page(s) 12578

Abstract: Among the most successful Lessepsian invaders is the symbiont-bearing benthic foraminifera Amphistegina lobifera. In its newly conquered habitat, this prolific calcifier and ecosystem engineer is exposed to environmental conditions that exceed the range ... ...

Abstract	Among the most successful Lessepsian invaders is the symbiont-bearing benthic foraminifera Amphistegina lobifera. In its newly conquered habitat, this prolific calcifier and ecosystem engineer is exposed to environmental conditions that exceed the range of its native habitat. To disentangle which processes facilitated the invasion success of A. lobifera into the Mediterranean Sea we analyzed a ~ 1400 bp sequence fragment covering the SSU and ITS gene markers to compare the populations from its native regions and along the invasion gradient. The genetic variability was studied at four levels: intra-genomic, population, regional and geographical. We observed that the invasion is not associated with genetic differentiation, but the invasive populations show a distinct suppression of intra-genomic variability among the multiple copies of the rRNA gene. A reduced genetic diversity compared to the Indopacific is observed already in the Red Sea populations and their high dispersal potential into the Mediterranean appears consistent with a bridgehead effect resulting from the postglacial expansion from the Indian Ocean into the Red Sea. We conclude that the genetic structure of the invasive populations reflects two processes: high dispersal ability of the Red Sea source population pre-adapted to Mediterranean conditions and a likely suppression of sexual reproduction in the invader. This discovery provides a new perspective on the cost of invasion in marine protists: The success of the invasive A. lobifera in the Mediterranean Sea comes at the cost of abandonment of sexual reproduction.
MeSH term(s)	Ecosystem ; Foraminifera/genetics ; Mediterranean Sea ; Indian Ocean ; Reproduction
Language	English
Publishing date	2023-08-03
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-39652-y
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Article ; Online: High variability in SSU rDNA gene copy number among planktonic foraminifera revealed by single-cell qPCR.

Milivojević, Tamara / Rahman, Shirin Nurshan / Raposo, Débora / Siccha, Michael / Kucera, Michal / Morard, Raphaël

ISME communications

2021 Volume 1, Issue 1, Page(s) 63

Abstract: Metabarcoding has become the workhorse of community ecology. Sequencing a taxonomically informative DNA fragment from environmental samples gives fast access to community composition across taxonomic groups, but it relies on the assumption that the ... ...

Abstract	Metabarcoding has become the workhorse of community ecology. Sequencing a taxonomically informative DNA fragment from environmental samples gives fast access to community composition across taxonomic groups, but it relies on the assumption that the number of sequences for each taxon correlates with its abundance in the sampled community. However, gene copy number varies among and within taxa, and the extent of this variability must therefore be considered when interpreting community composition data derived from environmental sequencing. Here we measured with single-cell qPCR the SSU rDNA gene copy number of 139 specimens of five species of planktonic foraminifera. We found that the average gene copy number varied between of ~4000 to ~50,000 gene copies between species, and individuals of the same species can carry between ~300 to more than 350,000 gene copies. This variability cannot be explained by differences in cell size and considering all plausible sources of bias, we conclude that this variability likely reflects dynamic genomic processes acting during the life cycle. We used the observed variability to model its impact on metabarcoding and found that the application of a correcting factor at species level may correct the derived relative abundances, provided sufficiently large populations have been sampled.
Language	English
Publishing date	2021-10-30
Publishing country	England
Document type	Journal Article
ISSN	2730-6151
ISSN (online)	2730-6151
DOI	10.1038/s43705-021-00067-3
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Article: Diverse Internal Symbiont Community in the Endosymbiotic Foraminifera

Schmidt, Christiane / Morard, Raphael / Romero, Oscar / Kucera, Michal

Frontiers in microbiology

2018 Volume 9, Page(s) 2018

Abstract: Many shallow-water tropical and subtropical foraminifera engage in photosymbiosis with eukaryotic microalgae. Some of these foraminifera appear to harbor a diverse consortium of endosymbiotic algae within a single host. Such apparent ability to contain ... ...

Abstract	Many shallow-water tropical and subtropical foraminifera engage in photosymbiosis with eukaryotic microalgae. Some of these foraminifera appear to harbor a diverse consortium of endosymbiotic algae within a single host. Such apparent ability to contain different symbionts could facilitate change in symbiont community composition (symbiont shuffling) and mediate the ecological success of the group in a changing environment. However, the discovery of the intra-individual symbiont diversity was thus far based on symbiont culturing, which provides strong constraints on the vitality of the identified algae but provides poor constraints on their initial abundance and thus functional relevance to the host. Here we analyze the algal symbiont diversity in
Language	English
Publishing date	2018-09-11
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2018.02018
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Article ; Online: Renewal of planktonic foraminifera diversity after the Cretaceous Paleogene mass extinction by benthic colonizers.

Morard, Raphaël / Hassenrück, Christiane / Greco, Mattia / Fernandez-Guerra, Antonio / Rigaud, Sylvain / Douady, Christophe J / Kucera, Michal

Nature communications

2022 Volume 13, Issue 1, Page(s) 7135

Abstract: The biotic crisis following the end-Cretaceous asteroid impact resulted in a dramatic renewal of pelagic biodiversity. Considering the severe and immediate effect of the asteroid impact on the pelagic environment, it is remarkable that some of the most ... ...

Abstract	The biotic crisis following the end-Cretaceous asteroid impact resulted in a dramatic renewal of pelagic biodiversity. Considering the severe and immediate effect of the asteroid impact on the pelagic environment, it is remarkable that some of the most affected pelagic groups, like the planktonic foraminifera, survived at all. Here we queried a surface ocean metabarcoding dataset to show that calcareous benthic foraminifera of the clade Globothalamea are able to disperse actively in the plankton, and we show using molecular clock phylogeny that the modern planktonic clades originated from different benthic ancestors that colonized the plankton after the end-Cretaceous crisis. We conclude that the diversity of planktonic foraminifera has been the result of a constant leakage of benthic foraminifera diversity into the plankton, continuously refueling the planktonic niche, and challenge the classical interpretation of the fossil record that suggests that Mesozoic planktonic foraminifera gave rise to the modern communities.
MeSH term(s)	Foraminifera/genetics ; Plankton/genetics ; Extinction, Biological ; Minor Planets ; Fossils
Language	English
Publishing date	2022-11-21
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-34794-5
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Article ; Online: Unassigned diversity of planktonic foraminifera from environmental sequencing revealed as known but neglected species.

Morard, Raphaël / Vollmar, Nele M / Greco, Mattia / Kucera, Michal

PloS one

2019 Volume 14, Issue 3, Page(s) e0213936

Abstract: Most research on extant planktonic foraminifera has been directed towards larger species (>0.150 mm) which can be easily manipulated, counted and yield enough calcite for geochemical analyses. This has drawn attention towards the macroperforate clade and ...

Abstract	Most research on extant planktonic foraminifera has been directed towards larger species (>0.150 mm) which can be easily manipulated, counted and yield enough calcite for geochemical analyses. This has drawn attention towards the macroperforate clade and created an impression of their numerical and ecological dominance. Drawing such conclusions from the study of such "giants" is a dangerous path. There were times in the evolutionary history of planktonic foraminifera when all species were smaller than 0.1 mm and indeed numerous small taxa, mainly from the microperforate clade, have been formally described from the modern plankton. The significance of these small, obscure and neglected species is poorly characterized and their relationship to the newly discovered hyperabundant but uncharacterized lineages of planktonic foraminifera in metabarcoding datasets is unknown. To determine, who is hiding in the metabarcoding datasets, we carried out an extensive sequencing of 18S rDNA targeted at small and obscure species. The sequences of the newly characterized small and obscure taxa match many of the previously uncharacterized lineages found in metabarcoding data. This indicates that most of the modern diversity in planktonic foraminifera has been taxonomically captured, but the role of the small and neglected taxa has been severely underestimated.
MeSH term(s)	Biodiversity ; DNA Barcoding, Taxonomic ; DNA, Protozoan/genetics ; Evolution, Molecular ; Foraminifera/classification ; Foraminifera/genetics ; Foraminifera/ultrastructure ; Microscopy, Electron, Scanning ; Phylogeny ; Phylogeography ; Plankton/classification ; Plankton/genetics ; Plankton/ultrastructure ; RNA, Ribosomal, 18S/genetics
Chemical Substances	DNA, Protozoan ; RNA, Ribosomal, 18S
Language	English
Publishing date	2019-03-21
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0213936
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