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Origin and the evolution of diatoms through the integration of paleontology and phylogenetics

Brylka, Karolina LU (2024) 41.
Abstract
Diatoms, the prominent photosynthetic eucaryotes, have inhabited the world’s oceans for at least the past 120 Ma since their first appearance in the Lower Cretaceous. There are also records of older diatoms, from the Jurassic dating to ca. 172 Ma and ca. 165 Ma, however these are poorly documented. The predicted origin time of diatoms using evolutionary relationships (molecular phylogenetics) yields an earlier date of origin of 200 Ma. These dates point towards some expected gaps in the fossil record, which may bias our understanding of early diatom evolution. Diatoms influence major geochemical cycles and sustain oceanic ecosystems in the modern ocean; hence, it is essential to learn about their past. To study diatom evolution across the... (More)
Diatoms, the prominent photosynthetic eucaryotes, have inhabited the world’s oceans for at least the past 120 Ma since their first appearance in the Lower Cretaceous. There are also records of older diatoms, from the Jurassic dating to ca. 172 Ma and ca. 165 Ma, however these are poorly documented. The predicted origin time of diatoms using evolutionary relationships (molecular phylogenetics) yields an earlier date of origin of 200 Ma. These dates point towards some expected gaps in the fossil record, which may bias our understanding of early diatom evolution. Diatoms influence major geochemical cycles and sustain oceanic ecosystems in the modern ocean; hence, it is essential to learn about their past. To study diatom evolution across the Mesozoic and Cenozoic time periods, scientists use two approaches: a traditional approach based on fossil record interpretation, and the more recently developed approach, which evolves around molecular and phylogenetic studies. This Ph.D. project is a combination of both approaches.

This thesis has the following objectives: (1) search for older diatom microfossils than previously described in the lower Cretaceous and Jurassic sediments, (2) revisit the oldest published diatom microfossils to establish their reliability, (3) analyze existing fossil information and progress the use of paleontology in phylogenetic studies, (4) reconstruct molecular evolution of environmentally responsive and an ecologically important gene family in diatoms. These objectives were addressed in four subprojects.

An extensive search for Lower Cretaceous and Jurassic diatoms discovered no new fossils. Instead, scarce sponge spicules and radiolarians were observed at several study sites and exhibited a high degree of dissolution and alteration. This finding suggests that diagenetic processes biased our observations, and potentially caused the complete absence of diatoms. The study of the oldest diatoms of the Lower and Middle Jurassic age revealed these fossils were not diatoms but most likely calcareous nannofossils and testate amoebae, respectively. This discovery extended the gap between the oldest fossils and estimated origin time to 80 million years. Moreover, we have shown the importance of careful evaluation of taxonomy, the elemental composition of the fossil, and the application of age control to establish the in-situ character of the fossil. The lack of diatoms in ancient sediments inspired further research on Cretaceous diatoms. To identify trends in distribution, diversity, and emergence of genera in time and space we compiled the Cretaceous Diatom Database. We identified extant diatom genera as far back as 100 million years and highlighted the importance of integrating these data into molecular tools. Diatoms in the Cretaceous are far more diverse then previously proposed, yet a substantial amount of taxonomical work is needed since many taxa were misclassified. Overall, based on the lower Cretaceous biogeographic dispersal and the morphological diversity of the oldest diatoms, together with diagenetic evidence from radiolarians and sponge spicules, we suggest that older diatoms than so far described are yet to be discovered.

We used molecular tools to unravel the evolution of diatoms, specifically genes responsible for silicon transport (SITs). This study focused on a diatom clade called Thalassiosirales, which has abundant representatives in the marine and freshwater realms-environments with varying levels of nutrients including dissolved silicon. Previous studies have shown that Thalassiosirales, both marine and freshwater, have multiple SITs which likely differ in their affinity and capacity for transport, moreover marine and freshwater diatoms exhibit differences in silicon metabolism. So far little evidence supports adaptive evolution on the sequence level, where diatom SITs have been shown to evolve predominantly under strong purifying selection. Advances in genome sequencing and updated codon models allowed us to formulate new questions and improve previous inferences. We showed extensive and ongoing history of gene duplication and loss. Furthermore, our data suggest the optimization of gene expression has played a central role in shaping sequence evolution and gene family dynamics of SITs, diatoms continuously balancing gene dosage and expression to optimize silicon transport across major environmental gradients.

This Ph.D. project was a multidisciplinary approach to study the evolution of diatoms. For certain studies, such as the evolution of SITs, molecular means were applicable, but to draw broad conclusions on the evolution of diatoms, it is crucial to combine the fossil record and phylogenetic studies. (Less)
Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Professor Beszteri, Bánk, University of Duisburg-Essen, Germany
organization
publishing date
type
Thesis
publication status
published
subject
keywords
diatoms, evolution, fossil record, Cretaceous, molecular evolution, Mesozoic, silicon transporter proteins, gene duplication
volume
41
edition
Litholund Thesis
pages
142 pages
publisher
Lund University, Faculty of Science, Department of Geology, Lithosphere and Biosphere Science
defense location
Pangea, Department of Geology, Sölvegatan 12, 223 62 Lund
defense date
2024-05-03 13:15:00
ISBN
978-91-87847-83-7
978-91-87847-82-0
language
English
LU publication?
yes
id
25b7d7d7-d68a-45f2-a1e8-943916d79c27
date added to LUP
2024-02-06 12:26:25
date last changed
2024-04-09 08:12:46
@phdthesis{25b7d7d7-d68a-45f2-a1e8-943916d79c27,
  abstract     = {{Diatoms, the prominent photosynthetic eucaryotes, have inhabited the world’s oceans for at least the past 120 Ma since their first appearance in the Lower Cretaceous. There are also records of older diatoms, from the Jurassic dating to ca. 172 Ma and ca. 165 Ma, however these are poorly documented. The predicted origin time of diatoms using evolutionary relationships (molecular phylogenetics) yields an earlier date of origin of 200 Ma. These dates point towards some expected gaps in the fossil record, which may bias our understanding of early diatom evolution. Diatoms influence major geochemical cycles and sustain oceanic ecosystems in the modern ocean; hence, it is essential to learn about their past. To study diatom evolution across the Mesozoic and Cenozoic time periods, scientists use two approaches: a traditional approach based on fossil record interpretation, and the more recently developed approach, which evolves around molecular and phylogenetic studies. This Ph.D. project is a combination of both approaches. <br/><br/>This thesis has the following objectives: (1) search for older diatom microfossils than previously described in the lower Cretaceous and Jurassic sediments, (2) revisit the oldest published diatom microfossils to establish their reliability, (3) analyze existing fossil information and progress the use of paleontology in phylogenetic studies, (4) reconstruct molecular evolution of environmentally responsive and an ecologically important gene family in diatoms. These objectives were addressed in four subprojects. <br/><br/>An extensive search for Lower Cretaceous and Jurassic diatoms discovered no new fossils. Instead, scarce sponge spicules and radiolarians were observed at several study sites and exhibited a high degree of dissolution and alteration. This finding suggests that diagenetic processes biased our observations, and potentially caused the complete absence of diatoms. The study of the oldest diatoms of the Lower and Middle Jurassic age revealed these fossils were not diatoms but most likely calcareous nannofossils and testate amoebae, respectively. This discovery extended the gap between the oldest fossils and estimated origin time to 80 million years. Moreover, we have shown the importance of careful evaluation of taxonomy, the elemental composition of the fossil, and the application of age control to establish the in-situ character of the fossil. The lack of diatoms in ancient sediments inspired further research on Cretaceous diatoms. To identify trends in distribution, diversity, and emergence of genera in time and space we compiled the Cretaceous Diatom Database. We identified extant diatom genera as far back as 100 million years and highlighted the importance of integrating these data into molecular tools. Diatoms in the Cretaceous are far more diverse then previously proposed, yet a substantial amount of taxonomical work is needed since many taxa were misclassified. Overall, based on the lower Cretaceous biogeographic dispersal and the morphological diversity of the oldest diatoms, together with diagenetic evidence from radiolarians and sponge spicules, we suggest that older diatoms than so far described are yet to be discovered. <br/><br/>We used molecular tools to unravel the evolution of diatoms, specifically genes responsible for silicon transport (SITs). This study focused on a diatom clade called Thalassiosirales, which has abundant representatives in the marine and freshwater realms-environments with varying levels of nutrients including dissolved silicon. Previous studies have shown that Thalassiosirales, both marine and freshwater, have multiple SITs which likely differ in their affinity and capacity for transport, moreover marine and freshwater diatoms exhibit differences in silicon metabolism. So far little evidence supports adaptive evolution on the sequence level, where diatom SITs have been shown to evolve predominantly under strong purifying selection. Advances in genome sequencing and updated codon models allowed us to formulate new questions and improve previous inferences. We showed extensive and ongoing history of gene duplication and loss. Furthermore, our data suggest the optimization of gene expression has played a central role in shaping sequence evolution and gene family dynamics of SITs, diatoms continuously balancing gene dosage and expression to optimize silicon transport across major environmental gradients. <br/><br/>This Ph.D. project was a multidisciplinary approach to study the evolution of diatoms. For certain studies, such as the evolution of SITs, molecular means were applicable, but to draw broad conclusions on the evolution of diatoms, it is crucial to combine the fossil record and phylogenetic studies.}},
  author       = {{Brylka, Karolina}},
  isbn         = {{978-91-87847-83-7}},
  keywords     = {{diatoms; evolution; fossil record; Cretaceous; molecular evolution; Mesozoic; silicon transporter proteins; gene duplication}},
  language     = {{eng}},
  month        = {{05}},
  publisher    = {{Lund University, Faculty of Science, Department of Geology, Lithosphere and Biosphere Science}},
  school       = {{Lund University}},
  title        = {{Origin and the evolution of diatoms through the integration of paleontology and phylogenetics}},
  url          = {{https://lup.lub.lu.se/search/files/177855790/Thesis_Karolina_Brylka_without_papers_LUCRIS.pdf}},
  volume       = {{41}},
  year         = {{2024}},
}