Is cyst formation in early eukaryotes a requirement for their preservation in the fossil record?

Most of the Archaean-Proterozoic fossil record consists of non-biomineralizing microorganisms or their signatures. Body fossils of bacteria and early eukaryotes are preserved in siliciclastics, shales and carbonates, and are usually studied by preparation of thin sections or extraction from the rock matrix via acid maceration.The first eukaryotic organic-walled microfossils (OWM) appear at least by 1.8 Ga and undergo morphological diversification and evolutionary radiation in the Mesoproterozoic. There are no preserved eukaryotic-grade microfossils except OWM until the onset of biomineralization much later in the Neoproterozoic, evident in the record of testate amoebae (VSM) and microfossils with scaly elements.OWM are a less conspicuous component of the fos-sil record than taxa with skeletal or shelly elements. Organic matter decays quickly upon death of the organism, due to autolytic enzymes or degradation via het-erotrophy. However, species producing vegetative cells, resting cysts, zygotes, or spores, show considerable resistance to autolysis. Case studies on extractable carbonaceous OWM indicate they are preserved due to complex refractory molecules in the structure of their sturdy vesicle walls. Living analogues across protistan clades utilise such sporopollenin-like compounds for the cyst wall construction during reproductive phase. Algaenan-containing trilaminar sheath structure (TLS) is secreted during aplanospore formation in extant chlorophyte alga Haematococcus. TLS has also been documented in Leiosphaeridia acritarchs from the Cambrian Lükati Formation in Estonia. Leiosphaeridia is a long ranging morphotype, dating as far back as 1.8 Ga. Presence of TLS in these fossils suggests their function as reproductive cyst. Dictyosphaera-Shuiyousphaeridium plexus from the Mesoproterozoic Ruyang Group, China, also exhibits cyst-like morphology and unique elements of wall reinforcement: internally secreted organic platelets.In addition to these early OWM, many Meso-Neoproterozoic taxa such as Tappania, Trachyhystrychosphaera and Kildinella contain cyst-like characters: 1) reproductive openings, 2) ornamentation, 3) occa-sionally preserved internal bodies and 4) acetolysis-resistant vesicle walls – properties observed among extant encysting protists.Ornamented (process-bearing) microfossils in par-ticular bear strong similarities with zygotes of living unicellular algae. Property of acetolysis-resistant vesicle is a result of sporopollenin-like macromolecules in the wall, synthesized most commonly by the autotrophic eukaryotes. Presence of such recalcitrant organic walls requires significant metabolic investment by the microorganism, which suggests a protective and/or reproductive function. This also allows for easier, and more detailed preservation in the rock record.One of the concerns arising from the studies on the early eukaryotic fossils is the bias towards encysting organisms. The eventual search for the fossil record on other planetary bodies could face the same challenges as the Precambrian palaeobiology: fossilisation and eventual detection might be problematic for any unicellular eukaryotic-grade organisms if they have not evolved reproduction via encystment, or cyst formation as means of coping with adverse environmental conditions.ORIGINS AND EARLY DIVERSIFICATION OF PHOTOSYNTHETIC MICROBIOT

Is cyst formation in early eukaryotes a requirement for their preservation in the fossil record?

Most of the Archaean-Proterozoic fossil record consists of non-biomineralizing microorganisms or their signatures. Body fossils of bacteria and early eukaryotes are preserved in siliciclastics, shales and carbonates, and are usually studied by preparation of thin sections or extraction from the rock matrix via acid maceration.The first eukaryotic organic-walled microfossils (OWM) appear at least by 1.8 Ga and undergo morphological diversification and evolutionary radiation in the Mesoproterozoic. There are no preserved eukaryotic-grade microfossils except OWM until the onset of biomineralization much later in the Neoproterozoic, evident in the record of testate amoebae (VSM) and microfossils with scaly elements.OWM are a less conspicuous component of the fos-sil record than taxa with skeletal or shelly elements. Organic matter decays quickly upon death of the organism, due to autolytic enzymes or degradation via het-erotrophy. However, species producing vegetative cells, resting cysts, zygotes, or spores, show considerable resistance to autolysis. Case studies on extractable carbonaceous OWM indicate they are preserved due to complex refractory molecules in the structure of their sturdy vesicle walls. Living analogues across protistan clades utilise such sporopollenin-like compounds for the cyst wall construction during reproductive phase. Algaenan-containing trilaminar sheath structure (TLS) is secreted during aplanospore formation in extant chlorophyte alga Haematococcus. TLS has also been documented in Leiosphaeridia acritarchs from the Cambrian Lükati Formation in Estonia. Leiosphaeridia is a long ranging morphotype, dating as far back as 1.8 Ga. Presence of TLS in these fossils suggests their function as reproductive cyst. Dictyosphaera-Shuiyousphaeridium plexus from the Mesoproterozoic Ruyang Group, China, also exhibits cyst-like morphology and unique elements of wall reinforcement: internally secreted organic platelets.In addition to these early OWM, many Meso-Neoproterozoic taxa such as Tappania, Trachyhystrychosphaera and Kildinella contain cyst-like characters: 1) reproductive openings, 2) ornamentation, 3) occa-sionally preserved internal bodies and 4) acetolysis-resistant vesicle walls – properties observed among extant encysting protists.Ornamented (process-bearing) microfossils in par-ticular bear strong similarities with zygotes of living unicellular algae. Property of acetolysis-resistant vesicle is a result of sporopollenin-like macromolecules in the wall, synthesized most commonly by the autotrophic eukaryotes. Presence of such recalcitrant organic walls requires significant metabolic investment by the microorganism, which suggests a protective and/or reproductive function. This also allows for easier, and more detailed preservation in the rock record.One of the concerns arising from the studies on the early eukaryotic fossils is the bias towards encysting organisms. The eventual search for the fossil record on other planetary bodies could face the same challenges as the Precambrian palaeobiology: fossilisation and eventual detection might be problematic for any unicellular eukaryotic-grade organisms if they have not evolved reproduction via encystment, or cyst formation as means of coping with adverse environmental conditions.ORIGINS AND EARLY DIVERSIFICATION OF PHOTOSYNTHETIC MICROBIOT

Is cyst formation in early eukaryotes a requirement for their preservation in the fossil record?

Most of the Archaean-Proterozoic fossil record consists of non-biomineralizing microorganisms or their signatures. Body fossils of bacteria and early eukaryotes are preserved in siliciclastics, shales and carbonates, and are usually studied by preparation of thin sections or extraction from the rock matrix via acid maceration.The first eukaryotic organic-walled microfossils (OWM) appear at least by 1.8 Ga and undergo morphological diversification and evolutionary radiation in the Mesoproterozoic. There are no preserved eukaryotic-grade microfossils except OWM until the onset of biomineralization much later in the Neoproterozoic, evident in the record of testate amoebae (VSM) and microfossils with scaly elements.OWM are a less conspicuous component of the fos-sil record than taxa with skeletal or shelly elements. Organic matter decays quickly upon death of the organism, due to autolytic enzymes or degradation via het-erotrophy. However, species producing vegetative cells, resting cysts, zygotes, or spores, show considerable resistance to autolysis. Case studies on extractable carbonaceous OWM indicate they are preserved due to complex refractory molecules in the structure of their sturdy vesicle walls. Living analogues across protistan clades utilise such sporopollenin-like compounds for the cyst wall construction during reproductive phase. Algaenan-containing trilaminar sheath structure (TLS) is secreted during aplanospore formation in extant chlorophyte alga Haematococcus. TLS has also been documented in Leiosphaeridia acritarchs from the Cambrian Lükati Formation in Estonia. Leiosphaeridia is a long ranging morphotype, dating as far back as 1.8 Ga. Presence of TLS in these fossils suggests their function as reproductive cyst. Dictyosphaera-Shuiyousphaeridium plexus from the Mesoproterozoic Ruyang Group, China, also exhibits cyst-like morphology and unique elements of wall reinforcement: internally secreted organic platelets.In addition to these early OWM, many Meso-Neoproterozoic taxa such as Tappania, Trachyhystrychosphaera and Kildinella contain cyst-like characters: 1) reproductive openings, 2) ornamentation, 3) occa-sionally preserved internal bodies and 4) acetolysis-resistant vesicle walls – properties observed among extant encysting protists.Ornamented (process-bearing) microfossils in par-ticular bear strong similarities with zygotes of living unicellular algae. Property of acetolysis-resistant vesicle is a result of sporopollenin-like macromolecules in the wall, synthesized most commonly by the autotrophic eukaryotes. Presence of such recalcitrant organic walls requires significant metabolic investment by the microorganism, which suggests a protective and/or reproductive function. This also allows for easier, and more detailed preservation in the rock record.One of the concerns arising from the studies on the early eukaryotic fossils is the bias towards encysting organisms. The eventual search for the fossil record on other planetary bodies could face the same challenges as the Precambrian palaeobiology: fossilisation and eventual detection might be problematic for any unicellular eukaryotic-grade organisms if they have not evolved reproduction via encystment, or cyst formation as means of coping with adverse environmental conditions.ORIGINS AND EARLY DIVERSIFICATION OF PHOTOSYNTHETIC MICROBIOT

Morphology of the Proterozoic eukaryotic microfossils as a reflection of their intracellular complexity

Mesoproterozoic is a time of increasing diversity of microscopic life and appearance of intricate new cell morphologies. First eukaryotes may have evolved around 2.4 Ga, but the first microbiota with intricate sculpture and ornamentation are found in the younger, 1.8.-1.6 Ga successions worldwide. Such microfossils were uncovered from the Ruyang Formation in Shanxi, China and Roper Group, Northern Territories, Australia, dating back to 1.6-1.0 Ga ago. Some of these unicellular organic-walled fossils share characters with Ediacaran and Phanerozoic fossils, as well as extant green microalgae. Key characters among some Precambrian acritarchs are acetolysis-resistant vesicle with multi-layered walls; vesicle ornamentation by diverse processes that are produced during cyst formation; and excystment openings for the release of gametes or daughter-cells. Combination of these morphological elements, also present in extant phytoplankton, reflects the fossils’ protective function as reproductive cysts, indicating that complex life cycles and reproduction were well under way in Mesoproterozoic. Several case studies of microfossil morphology likely induced by intrinsic eukaryotic mechanisms are presented. Distinctive vesicle wall composed of the primary layer reinforced by polygonal platelets in Mesoproterozoic taxa Dictyosphaera and Shuiyouisphaeridium, as well as the sophisticated vesicle-wall patterning on the fossil sphaeromorphs Valeria and younger Cerebrosphaera would have required a certain degree of complexity for their formation, as observed in the present day analogues among eukaryotic protists. This suggests the activity of the key eukaryotic organelles and cellular mechanisms and signalling for the cyst formation. Considering that Golgi apparatus and the endoplasmatic reticulum are the organelles regulating eukaryotic secretory pathway and synthesis of biopolymers used in cell-wall construction, they would have been required for the complex morphology observed in these Precambrian taxa. Therefore, the presence of GA and ER in the eukaryotic cell is inferred at the minimum age of 1.6-1.4 Ga. Similarly, morphology of acritarchs of the Cambrian galeate plexus, namely openings with opercula, is likely induced by the activity of the LFA organelle (lid-forming apparatus) as in the extant dasycladalean alga Acetabularia. Additionally, several new morphotypes from the Ruyang Formation are presented. These unicellular fossils bear a velutinous outer membrane surrounding an internal sphere, which suggests a protective function of a reproductive or a resting cyst. Cyst-like morphology varies in disparity, but its key features are consistent through Mesoproterozoic, Neoproterozoic and early Palaeozoic

Morphology of the Proterozoic eukaryotic microfossils as a reflection of their intracellular complexity

Mesoproterozoic is a time of increasing diversity of microscopic life and appearance of intricate new cell morphologies. First eukaryotes may have evolved around 2.4 Ga, but the first microbiota with intricate sculpture and ornamentation are found in the younger, 1.8.-1.6 Ga successions worldwide. Such microfossils were uncovered from the Ruyang Formation in Shanxi, China and Roper Group, Northern Territories, Australia, dating back to 1.6-1.0 Ga ago. Some of these unicellular organic-walled fossils share characters with Ediacaran and Phanerozoic fossils, as well as extant green microalgae. Key characters among some Precambrian acritarchs are acetolysis-resistant vesicle with multi-layered walls; vesicle ornamentation by diverse processes that are produced during cyst formation; and excystment openings for the release of gametes or daughter-cells. Combination of these morphological elements, also present in extant phytoplankton, reflects the fossils’ protective function as reproductive cysts, indicating that complex life cycles and reproduction were well under way in Mesoproterozoic. Several case studies of microfossil morphology likely induced by intrinsic eukaryotic mechanisms are presented. Distinctive vesicle wall composed of the primary layer reinforced by polygonal platelets in Mesoproterozoic taxa Dictyosphaera and Shuiyouisphaeridium, as well as the sophisticated vesicle-wall patterning on the fossil sphaeromorphs Valeria and younger Cerebrosphaera would have required a certain degree of complexity for their formation, as observed in the present day analogues among eukaryotic protists. This suggests the activity of the key eukaryotic organelles and cellular mechanisms and signalling for the cyst formation. Considering that Golgi apparatus and the endoplasmatic reticulum are the organelles regulating eukaryotic secretory pathway and synthesis of biopolymers used in cell-wall construction, they would have been required for the complex morphology observed in these Precambrian taxa. Therefore, the presence of GA and ER in the eukaryotic cell is inferred at the minimum age of 1.6-1.4 Ga. Similarly, morphology of acritarchs of the Cambrian galeate plexus, namely openings with opercula, is likely induced by the activity of the LFA organelle (lid-forming apparatus) as in the extant dasycladalean alga Acetabularia. Additionally, several new morphotypes from the Ruyang Formation are presented. These unicellular fossils bear a velutinous outer membrane surrounding an internal sphere, which suggests a protective function of a reproductive or a resting cyst. Cyst-like morphology varies in disparity, but its key features are consistent through Mesoproterozoic, Neoproterozoic and early Palaeozoic

Morphology of the Proterozoic eukaryotic microfossils as a reflection of their intracellular complexity

Mesoproterozoic is a time of increasing diversity of microscopic life and appearance of intricate new cell morphologies. First eukaryotes may have evolved around 2.4 Ga, but the first microbiota with intricate sculpture and ornamentation are found in the younger, 1.8.-1.6 Ga successions worldwide. Such microfossils were uncovered from the Ruyang Formation in Shanxi, China and Roper Group, Northern Territories, Australia, dating back to 1.6-1.0 Ga ago. Some of these unicellular organic-walled fossils share characters with Ediacaran and Phanerozoic fossils, as well as extant green microalgae. Key characters among some Precambrian acritarchs are acetolysis-resistant vesicle with multi-layered walls; vesicle ornamentation by diverse processes that are produced during cyst formation; and excystment openings for the release of gametes or daughter-cells. Combination of these morphological elements, also present in extant phytoplankton, reflects the fossils’ protective function as reproductive cysts, indicating that complex life cycles and reproduction were well under way in Mesoproterozoic. Several case studies of microfossil morphology likely induced by intrinsic eukaryotic mechanisms are presented. Distinctive vesicle wall composed of the primary layer reinforced by polygonal platelets in Mesoproterozoic taxa Dictyosphaera and Shuiyouisphaeridium, as well as the sophisticated vesicle-wall patterning on the fossil sphaeromorphs Valeria and younger Cerebrosphaera would have required a certain degree of complexity for their formation, as observed in the present day analogues among eukaryotic protists. This suggests the activity of the key eukaryotic organelles and cellular mechanisms and signalling for the cyst formation. Considering that Golgi apparatus and the endoplasmatic reticulum are the organelles regulating eukaryotic secretory pathway and synthesis of biopolymers used in cell-wall construction, they would have been required for the complex morphology observed in these Precambrian taxa. Therefore, the presence of GA and ER in the eukaryotic cell is inferred at the minimum age of 1.6-1.4 Ga. Similarly, morphology of acritarchs of the Cambrian galeate plexus, namely openings with opercula, is likely induced by the activity of the LFA organelle (lid-forming apparatus) as in the extant dasycladalean alga Acetabularia. Additionally, several new morphotypes from the Ruyang Formation are presented. These unicellular fossils bear a velutinous outer membrane surrounding an internal sphere, which suggests a protective function of a reproductive or a resting cyst. Cyst-like morphology varies in disparity, but its key features are consistent through Mesoproterozoic, Neoproterozoic and early Palaeozoic

Data from: Affinity, life cycle, and intracellular complexity of organic-walled 2 microfossils from the Mesoproterozoic of Shanxi, China

Light microscope and scanning electron microscope observations on new material of unicellular microfossils Dictyosphaera macroreticulata and Shuiyousphaeridium macroreticulatum, from the Mesoproterozoic Ruyang Group in China, provide insights into the microorganisms’ biological affinity, life cycle and cellular complexity. Gigantosphaeridium fibratum n. gen. et sp., is described and is one of the largest Mesoproterozoic microfossils recorded. Phenotypic characters of vesicle ornamentation and excystment structures, properties of resistance and cell wall structure in Dictyosphaera and Shuiyousphaeridium are all diagnostic of microalgal cysts. The wide size ranges of the various morphotypes indicate growth phases compatible with the development of reproductive 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 a reproductive strategy of alternation of heteromorphic generations. Similarly in Gigantosphaeridium, a metabolically expensive vesicle with processes suggests its protective role as a zygotic cyst. In combination with all these characters and from the resemblance to extant green algae, we propose the placement of these ancient microorganisms in the stem group of Chloroplastida (Viridiplantae). A cell wall composed of primary and secondary layers in Dictyosphaera and Shuiyouisphaeridium required a high cellular complexity for their synthesis and the presence of an endomembrane system and the Golgi apparatus. The plastid was also present, accepting the organism was photosynthetic. The biota reveals a high degree of morphological and cell structural complexity, and provides an insight into ongoing eukaryotic evolution and the development of complex life cycles with sexual reproduction by 1200 Ma

Authors' Note for Agić et al. JoP

Note on the new age constraints on the Ruyang Formation, published in Lan et al. 2014 (Precambrian Research) after the submission and acceptance of this manuscript