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Palaeobiology and diversification of Proterozoic-Cambrian photosynthetic eukaryotes
Uppsala University, Disciplinary Domain of Science and Technology, Earth Sciences, Department of Earth Sciences, Palaeobiology. (ORIGINS AND EARLY DIVERSIFICATION OF PHOTOSYNTHETIC MICROBIOTA)
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

One of the most important events in the history of life is the evolution of the complex, eukaryotic cell. The eukaryotes are complex organisms with membrane-bound intracellular structures, and they include a variety of both single-celled and multicellular organisms: plants, animals, fungi and various protists. The evolutionary origin of this group may be studied by direct evidence of past life: fossils. The oldest traces of eukaryotes have appeared by 2.4 billion years ago (Ga), and have additionally diversified in the period around 1.8 Ga. The Mesoproterozoic Era (1.6-1 Ga) is characterised by the first evidence of the appearance complex unicellular microfossils, as well as innovative morphologies, and the evolution of sexual reproduction and multicellularity. For a better understanding of the early eukaryotic evolution and diversification patterns, a part of this thesis has focused on the microfossil records from various time periods and geographic locations. Examination of microfossil morphology, cell wall microstructure and biochemical properties, reflect their intracellular complexity and function, and allow reconstructions of their life cycle, as well as observing the evolutionary pattern of change from Mesoproterozoic, to Cambrian-Ordovician transition. Several case studies included assemblages deriving from Mesoproterozoic, Neoproterozoic and early Paleozoic time intervals that show disparate morphotypes and innovative features indicative of algal clades. The Mesoproterozoic Ruyang Group in northern China has yielded a diverse microfossil assemblage that provides important clues about the diversification of different eukaryotic groups. Furthermore these microfossils contributed an additional evidence for the emergence of the crown group Eukarya by 1.7-1.4 Ga. In another part of this thesis, examination of wall microstructure and chemical properties via Raman spectroscopy has been used to assess the biological affinities of various Neoproterozoic problematic carbonaceous compression fossils. Studies on the early Phanerozoic (c. 545-485 Ma) assemblages from Estonia reconstructed patterns of the early radiations of phytoplankton and its evolutionary innovations. A continuing theme in this thesis has been using a combination of evidence of microfossils’ fine-scale morphology, ecology and chemical properties to determine their function in life, in addition to their systematic position.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. , 47 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1308
Keyword [en]
microfossils, eukaryotes, Mesoproterozoic, Neoproterozoic, Cambrian, Ordovician, palaeobiology, biostratigraphy, phylogeny, China, Estonia, Siberian Platform, prasinophytes, microstructure, Raman spectroscopy
National Category
Geology
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
URN: urn:nbn:se:uu:diva-265229ISBN: 978-91-554-9389-9 (print)OAI: oai:DiVA.org:uu-265229DiVA: diva2:864160
Public defence
2015-12-11, Hambergsalen, Geocentrum, Villavägen 16, 752 36, Uppsala, 10:15 (English)
Opponent
Supervisors
Projects
Palaeobiology and diversification of Proterozoic-Cambrian photosynthetic eukaryotes
Funder
Swedish Research Council, 621-2009-4445
Available from: 2015-11-19 Created: 2015-10-26 Last updated: 2016-01-13
List of papers
1. Affnity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi, China
Open this publication in new window or tab >>Affnity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi, China
2015 (English)In: Journal of Paleontology, ISSN 0022-3360, E-ISSN 1937-2337, Vol. 89, no 1, 28-50 p.Article in journal (Refereed) Published
Abstract [en]

Light microscope and scanning electron microscope observations on new material of unicellularmicrofossils Dictyosphaera macroreticulata and Shuiyousphaeridium macroreticulatum, from the MesoproterozoicRuyang Group in China, provide insights into the microorganisms’ biological affinity, life cycle and cellularcomplexity. Gigantosphaeridium fibratum n. gen. et sp., is described and is one of the largest Mesoproterozoicmicrofossils recorded. Phenotypic characters of vesicle ornamentation and excystment structures, properties ofresistance and cell wall structure in Dictyosphaera and Shuiyousphaeridium are all diagnostic of microalgalcysts. The wide size ranges of the various morphotypes indicate growth phases compatible with the development ofreproductive cysts. Conspecific biologically, each morphotype represents an asexual (resting cyst) or sexual (zygotic cyst)stage in the life cycle, respectively. We reconstruct this hypothetical life cycle and infer that the organism demonstrates areproductive strategy of alternation of heteromorphic generations. Similarly in Gigantosphaeridium, a metabolicallyexpensive vesicle with processes suggests its protective role as a zygotic cyst. In combination with all these charactersand from the resemblance to extant green algae, we propose the placement of these ancient microorganisms in the stemgroup of Chloroplastida (Viridiplantae). A cell wall composed of primary and secondary layers in Dictyosphaera andShuiyouisphaeridium required a high cellular complexity for their synthesis and the presence of an endomembranesystem and the Golgi apparatus. The plastid was also present, accepting the organism was photosynthetic. The biotareveals a high degree of morphological and cell structural complexity, and provides an insight into ongoing eukaryoticevolution and the development of complex life cycles with sexual reproduction by 1200Ma.

Place, publisher, year, edition, pages
Cambridge Journals, 2015
Keyword
organic-walled microfossils; early eukaryotes; Mesoproterozoic; Dictyosphaera; Shuiyousphaeridium; algae; evolution; intracellular complexity
National Category
Geology
Research subject
Earth Science with specialization in Historical Geology and Palaeontology; Biology with specialization in Systematics
Identifiers
urn:nbn:se:uu:diva-247264 (URN)10.1017/jpa.2014.4 (DOI)000351478500003 ()
Funder
Swedish Research Council, 621-2009-4445
Available from: 2015-03-16 Created: 2015-03-16 Last updated: 2017-12-04Bibliographically approved
2. Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang Group, North China Craton - a window into the early eukaryote evolution
Open this publication in new window or tab >>Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang Group, North China Craton - a window into the early eukaryote evolution
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Mesoproterozoic Era was an important time for the initial diversification of eukaryotic groups and the appearance of the first complex morphologies. While eukaryotes evolved around 2.4 Ga, the first microfossils with ornamentation and sculpture occur in the 1.8-1.6 Ga successions worldwide. Shales and siltstones of the Ruyang Group, Shanxi Province, North China Craton, record a high diversity of such organic-walled microfossils. Recently, the depositional ages of this succession has been constrained to 1.75-1.40 Ga via   zircon U-Pb dating. This dating extends back the time of the first appearance of complex eukaryotic characters (e.g. processes, complex wall structure) in the fossil record. We have conducted a biostratigraphic investigation on of the samples throughout the fossiliferous Ruyang Group to provide an estimate of the early eukaryotic diversity in the Mesoproterozoic. Light- and scanning electron microscope studies have documented 26 species, including several that are reported for the first time, and some that were previously known only from younger, Neoproterozoic strata. Fossil diversity is high in the upper Baicaoping Formation, declines in the middle and reaches its peak in the upper Beidajian Formation. Novel morphologies among the unicellular Ruyang biota include a variety of processes, from tube-like extensions to hirsute spines, vesicles with velutinous outer membranes, as well as numerous specimens with internal bodies of varying sizes. We have also recorded the globally distributed Mesoproterozoic taxa Dictyosphaera, Shuiyousphaeridium, and Tappania. Key characters displayed by the Ruyang biota are consistent with reproductive structures (especially cysts among modern protists. These microfossils provide an additional evidence for the emergence of the crown group Eukarya by 1.7-1.4 Ga.

Keyword
Mesoproterozoic, Ruyang Group, organic-walled microfossils, eukaryotic evolution, North China, Dictyosphaera.
National Category
Natural Sciences Geology
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
urn:nbn:se:uu:diva-265216 (URN)
Projects
Palaeobiology and diversification of Proterozoic-Cambrian photosynthetic eukaryotes
Funder
Swedish Research Council, 621-2009-4445
Available from: 2015-10-25 Created: 2015-10-25 Last updated: 2015-12-04
3. Raman spectroscopy and microstructural comparison of carbonaceous compression and body fossils from the Neoproterozoic of Siberian and Eastern European platforms
Open this publication in new window or tab >>Raman spectroscopy and microstructural comparison of carbonaceous compression and body fossils from the Neoproterozoic of Siberian and Eastern European platforms
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Macroscopic, organic-walled fossils preserved as carbonaceous compressions and body fossils are commonly occurring in the Neoproterozoic-Cambrian successions worldwide. Most of these fossils, including studied here Chuaria, Tawuia, and Beltemelliformis, have been accepted as algae, and Sabellidites as an early metazoan. They possess limited characters for biological identification and differ in gross morphology of spherodial vs. tubular millimetre-sized specimens. Consequently, other methods than morphologic observations are needed to elucidate their affinities and, ultimately, phylogeny. Here we present a comparison of the Raman spectrographic signatures and new scanning electron microscope (SEM) observations on different carbonaceous compression and body fossils from the Khajpakh Formation (Siberian Platform), and Nekrasovo Formation (East European Platform), referred to the Tonian-Cryogenian transitional interval (c. 840-700 Ma) and the lowermost Cambrian stage, respectively. Data from the Raman spectroscopy of the walls of non-mineralised organisms reveal their chemical properties, and, in additions to microstructural characters, may be used to resolve the fossils’ phylogenetic affinities. To test the basic recognition of organic matter in studied photosynthetic organisms vs. animals, we have examined algal compression fossils and organically-preserved body-fossil. Differences in the Raman spectroscopic signature between various taxa have been observed. Vibrational absorption bands similar to those characteristic of α-chitin signature have been detected in the organic wall of Sabellidites, consistent with its metazoan identity. Distinct organic matter spectra of the macroalgae Chuaria, Tawuia and Beltanelliformis, and the possible early annelid Sabellidites indicate that Raman spectroscopy could be a useful method in identifying different branches of the early eukaryotes. Additionally, the recognition of the earliest metazoans among un-diagnostic tubular fossils by biochemical signatures and wall ultrastructure, could provide the minimum age of their origins.

Keyword
Neoproterozoic, Cambrian, tubular fossils, organic body fossils, Raman spectroscopy, SEM, East European Platform, Siberian Platform
National Category
Natural Sciences Geology
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
urn:nbn:se:uu:diva-265206 (URN)
Projects
Palaeobiology and diversification of Proterozoic-Cambrian photosynthetic eukaryotes
Funder
Swedish Research Council, 621-2012-1669
Available from: 2015-10-25 Created: 2015-10-25 Last updated: 2015-12-04
4. Ecdysozoan-like sclerites among Ediacaran microfossils
Open this publication in new window or tab >>Ecdysozoan-like sclerites among Ediacaran microfossils
2015 (English)In: Geological Magazine, ISSN 0016-7568, E-ISSN 1469-5081, Vol. 152, no 6, 1145-1148 p.Article in journal (Refereed) Published
Abstract [en]

We report the occurrence of organically preserved microfossils from the subsurface Ediacaran strata overlying the East European Platform in Poland, in the form of sclerites and cuticle fragments of larger organisms. They are morphologically similar to those known from Cambrian strata and associated with various metazoan fossils of recognized phyla. The Ediacaran age of the microfossils is evident from the stratigraphic position below the base of the Cambrian System and above the isotopically dated tuff layers at c. 551±4Ma. Within this strata interval, other characteristic Ediacaran microorganisms co-occur such as cyanobacteria, vendotaenids, microalgae, Ceratophyton,Valkyria and macroscopic annelidan Sabellidites. The recent contributions of organic sclerites in revealing the scope of the Cambrian explosion are therefore also potentially extendable back to the Ediacaran Period when animals first appear in the fossil record.

Place, publisher, year, edition, pages
Cambridge: Cambridge University Press, 2015
Keyword
Ediacaran metazoans; small carbonaceous fossils; Poland; organic preservation; refractory biopolymers
National Category
Geology
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
urn:nbn:se:uu:diva-264156 (URN)10.1017/S001675681500045X (DOI)000367730400013 ()
Funder
Swedish Research Council, 621-2012-1669, 621-2011-4703
Available from: 2015-10-06 Created: 2015-10-06 Last updated: 2017-12-01Bibliographically approved
5. A new species of small acritarch with porous wall structure from the early Cambrian of Estonia, and implications for the fossil record of eukaryotic picoplankton
Open this publication in new window or tab >>A new species of small acritarch with porous wall structure from the early Cambrian of Estonia, and implications for the fossil record of eukaryotic picoplankton
2015 (English)In: Palynology, ISSN 0191-6122, E-ISSN 1558-9188, Vol. 40, no 3, 343-356 p.Article in journal (Refereed) Published
Abstract [en]

The Proterozoic-Phanerozoic transition records a general trend of decrease in phytoplankton cell size, in contrast tothe earlier and much larger Ediacaran acritarchs. Particularly minute, unornamented but sculptured organic-walledmicrofossils have been recovered from the lower Cambrian Lükati Formation in northern Estonia. The lack of anysignificant thermal alteration in the formation allowed for excellent preservation of fine microstructures on thesemicrofossils. Among the rich palynomorph assemblage in Lükati, a new species of tiny, spheroidal eukaryoticmicrofossil is recorded: Reticella corrugata gen. et sp. nov. It is characterised by a corrugated and flexible vesicle wallthat is densely perforated by nano-scale pores. Despite its unique morphology, the new species shares diagnosticcharacters with fossil and extant prasinophyte algae. R. corrugata is among the smallest microfossils with typicaleukaryotic morphology (conspicuous wall sculpture) and contributes to the diversity of the size class of smallacritarchs. Size, abundance, inferred prasinophyte affinity and eukaryotic wall sculpture make this new taxon alikely member of the early eukaryotic picoplankton.

Keyword
Cambrian, Estonia, organic-walled microfossils, picoplankton, prasinophytes, small acritarchs
National Category
Geology Ecology
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
urn:nbn:se:uu:diva-265208 (URN)10.1080/01916122.2015.1068879 (DOI)000386047200007 ()
Projects
Palaeobiology and diversification of Proterozoic-Cambrian photosynthetic eukaryotes
Funder
Swedish Research Council, 621-2012-1669
Available from: 2015-10-25 Created: 2015-10-25 Last updated: 2017-11-10Bibliographically approved
6. Reproductive cyst and operculum formation in the Cambrian-Ordovician galeate-plexus microfossils
Open this publication in new window or tab >>Reproductive cyst and operculum formation in the Cambrian-Ordovician galeate-plexus microfossils
2016 (English)In: GFF, ISSN 1103-5897, E-ISSN 2000-0863, Vol. 138, no 2, 278-294 p.Article in journal (Refereed) Published
Abstract [en]

Unicellular organic-walled microfossils from the Cambrian-Ordovician transition in Estonia (ca. 490-480 million years ago) exhibit rare characters reflecting their function as reproductive algal cysts. The studied assemblages record the evolutionary history of phytoplankton in the early Paleozoic Era: novel morphologies appearing through the Cambrian and subsequently diversifying in the Ordovician. Well preserved specimens were extracted following a standard palynological method and studied by light transmitted microscopy. The galeate plexus acritarchs Caldariola, Priscogalea and Stelliferidium have revealed exceptionally preserved morphological elements and a rare structure among both fossil and extant protists – an opening with operculum (lid) in reproductive cysts, in addition to lavish vesicle ornamentation and sculpture. Analogous morphology is observed in the living dasycladalean alga Acetabularia (Chlorophyta), which possesses an intrinsic lid-forming apparatus used during organism’s reproductive stage. Based on the observations on the fossil material and studies on the Acetabularia lid-formation, we propose a model of operculum formation in the galeate plexus microorganisms. Due to strong morphological and ecological similarities between galeate fossils and dasycladalean cysts, and the antiquity of this algal order, galeates may be positioned within green algae, more specifically Dasycladales. Unique morphology of the operculum-bearing microbiota would have required a high degree of intracellular complexity for its development, suggesting that advanced intracellular machinery was present already in the early Paleozoic phytoplankton. Additionally, minute prasinophyte microfossils Reticella corrugata  are reported for the first time in the Upper Cambrian strata. 

Keyword
acritarchs, Baltica, cyst-formation, Dasycladales, Estonia, galeate plexus, microfossils, operculum, Ordovician, palaeobiology
National Category
Geology Botany
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
urn:nbn:se:uu:diva-265207 (URN)10.1080/11035897.2015.1116603 (DOI)000379763500001 ()
Projects
Palaeobiology and diversification of Proterozoic-Cambrian photosynthetic eukaryotes
Funder
Swedish Research Council, 621-2012-1669Danish National Research Foundation, DNRF53
Available from: 2015-10-25 Created: 2015-10-25 Last updated: 2017-12-01Bibliographically approved

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