The Geological Succession of Primary Producers in the Oceans

Knoll, Andrew H.; Summons, Roger E.; Waldbauer, Jacob R.; Zumberge, John E.

doi:10.1016/b978-012370518-1/50009-6

Cited by 179 publications

(189 citation statements)

References 147 publications

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“…S4). This result makes sense, because our divergence time estimates imply that the evolution of the 3HP bicycle occurred after Cyanobacteria and even algae came to dominate primary productivity globally in most ecosystems (32). It additionally suggests that, although the 3HP bicycle is both energetically efficient and insensitive to dioxygen-features that make it unique from all other carbon fixation pathways-one of the reasons it was never used for oxygenic photosynthesis may have been because it wasn't present during the radiation of Cyanobacteria and the emergence of plastids.…”

Section: Resultsmentioning

confidence: 86%

Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

Shih

Ward

Fischer

2017

Proc. Natl. Acad. Sci. U.S.A.

103

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Various lines of evidence from both comparative biology and the geologic record make it clear that the biochemical machinery for anoxygenic photosynthesis was present on early Earth and provided the evolutionary stock from which oxygenic photosynthesis evolved ca. 2.3 billion years ago. However, the taxonomic identity of these early anoxygenic phototrophs is uncertain, including whether or not they remain extant. Several phototrophic bacterial clades are thought to have evolved before oxygenic photosynthesis emerged, including the Chloroflexi, a phylum common across a wide range of modern environments. Although Chloroflexi have traditionally been thought to be an ancient phototrophic lineage, genomics has revealed a much greater metabolic diversity than previously appreciated. Here, using a combination of comparative genomics and molecular clock analyses, we show that phototrophic members of the Chloroflexi phylum are not particularly ancient, having evolved well after the rise of oxygen (ca. 867 million years ago), and thus cannot be progenitors of oxygenic photosynthesis. Similarly, results show that the carbon fixation pathway that defines this clade-the 3-hydroxypropionate bicycleevolved late in Earth history as a result of a series of horizontal gene transfer events, explaining the lack of geological evidence for this pathway based on the carbon isotope record. These results demonstrate the role of horizontal gene transfer in the recent metabolic innovations expressed within this phylum, including its importance in the development of a novel carbon fixation pathway.carbon fixation | phototrophy | molecular clock | comparative genomics F rom both biological and geological data, it is widely thought that anoxygenic photosynthesis preceded the development of oxygenic photosynthesis and the rise of atmospheric oxygen (1). Although it has been largely accepted that oxygenic photosynthesis evolved in ancient Cyanobacterial lineages (2), very little is known about the nature and evolutionary history of anoxygenic phototrophy, with most of our understanding stemming from assumptions and hypotheses based on the few extant bacterial taxa that host this metabolism. Given the significance of the accumulation of oxygen ca. ∼2.3 billion years ago, it is of no surprise that the majority of efforts have focused on studying oxygenic photosynthesis. However, this has resulted in a paucity of studies critically examining basic and core questions on the origins of anoxygenic photosynthesis, such as what bacterial lineage developed this metabolism and when did it evolve? These questions are essential to our first-order knowledge of how early microbial metabolisms may have shaped the geochemical cycles of our planet.Although chlorophyll-based photosynthesis can be found in seven known bacterial phyla (i.e

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Section: Resultsmentioning

confidence: 86%

Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

Shih

Ward

Fischer

2017

Proc. Natl. Acad. Sci. U.S.A.

103

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“…Paradoxically, the sedimentary context of the 2-methylhopane fossil record suggests ancient 2-MeBHP producers inhabited shallow, tropical marine environments (Knoll et al, 2007). It is noteworthy that our culture-independent search for hpnP sequences in all marine metagenomes, highly biased towards open water, coastal and estuarine samples, did not identify any cyanobacterial hpnP sequences.…”

Section: -Mebhp Production Is Niche Specific Jn Ricci Et Almentioning

confidence: 76%

“…In fact, 2-methylhopanes have a rich history in the fossil record, found at discrete times and locations as far back as 2.7 billion years (Brocks et al, 1999), although this latter finding is under scrutiny (Rasmussen et al, 2008). The varied distribution of 2-methylhopanes in the more 'recent' rock record (that is, million-year timescales), showing peaks in abundance correlated with ocean anoxic events, suggests their production may be linked to particular environmental triggers (Knoll et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche

et al. 2013

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Molecular fossils of 2-methylhopanoids are prominent biomarkers in modern and ancient sediments that have been used as proxies for cyanobacteria and their main metabolism, oxygenic photosynthesis. However, substantial culture and genomic-based evidence now indicates that organisms other than cyanobacteria can make 2-methylhopanoids. Because few data directly address which organisms produce 2-methylhopanoids in the environment, we used metagenomic and clone library methods to determine the environmental diversity of hpnP, the gene encoding the C-2 hopanoid methylase. Here we show that hpnP copies from alphaproteobacteria and as yet uncultured organisms are found in diverse modern environments, including some modern habitats representative of those preserved in the rock record. In contrast, cyanobacterial hpnP genes are rarer and tend to be localized to specific habitats. To move beyond understanding the taxonomic distribution of environmental 2-methylhopanoid producers, we asked whether hpnP presence might track with particular variables. We found hpnP to be significantly correlated with organisms, metabolisms and environments known to support plant-microbe interactions (P-valueo10 À 6 ); in addition, we observed diverse hpnP types in closely packed microbial communities from other environments, including stromatolites, hot springs and hypersaline microbial mats. The common features of these niches indicate that 2-methylhopanoids are enriched in sessile microbial communities inhabiting environments low in oxygen and fixed nitrogen with high osmolarity. Our results support the earlier conclusion that 2-methylhopanoids are not reliable biomarkers for cyanobacteria or any other taxonomic group, and raise the new hypothesis that, instead, they are indicators of a specific environmental niche.

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“…It is now ambiguous as it is not restricted only to dinoflagellates. This could explain the presence of dinosteranes in sediment bulk samples from Archaean (Brocks et al, 2003), Proterozoic, and Cambrian ages (Summons et al, 1992;Peng et al, 1998;Moldowan and Talyzina, 1998;Moldowan et al, 2001;Knoll et al, 2007), well before the appearance of dinoflagellates in the Permian-Mesozoic rock record (Fensome et al, 1996). If resistant dinosteranes were derived from dinocysts, fossils would have been preserved; therefore the absence of dinocysts is less likely to be due to their poor preservation potential.…”

Section: Biological Affinity Of Dictyosphaerashuiyousphaeridium Plexusmentioning

confidence: 99%

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

Agić¹,

Moczydłowska²,

Yin

2015

J. Paleontol.

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Abstract.-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.

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The Geological Succession of Primary Producers in the Oceans

Cited by 179 publications

References 147 publications

Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche

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

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