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• W2785681605 abstract "•A Tonian (∼1,000–720 Ma) akinete-bearing filamentous cyanobacterium is reported•The fossil is inferred to have been a benthic microbial mat constructor•It is a heterocystous nitrogen-fixing cyanobacterium belonging to subsections IV+V•It helps to calibrate the rise of complex multicellularity in cyanobacteria Cyanobacteria were the ultimate ancestor of all plastids and, for much of Earth’s history, the only source of biogenic oxygen and a major source of fixed carbon and nitrogen. One cyanobacterial clade, subsections IV+V, is characterized by multicellularity and cell differentiation, with many members bearing specialized nitrogen-fixing (or diazotrophic) heterocysts and encysting akinetes [1Adams D.G. Duggan P.S. Heterocyst and akinete differentiation in cyanobacteria.New Phytol. 1999; 144: 3-33Crossref Scopus (194) Google Scholar, 2Castenholz R.W. Cyanobacteria: oxygenic photosynthetic bacteria.in: Boone D.R. Castenholz R.W. Garrity G.M. Bergey’s Manual of Systematic Bacteriology. Second Edition. Volume 1. Springer, New York2001: 473-599Crossref Google Scholar, 3Tomitani A. Knoll A.H. Cavanaugh C.M. Ohno T. The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives.Proc. Natl. Acad. Sci. USA. 2006; 103: 5442-5447Crossref PubMed Scopus (338) Google Scholar]. Molecular clock estimates of the divergence time of this clade are highly variable, ranging from ∼2,000 Ma (mega-annum) [4Schirrmeister B.E. Gugger M. Donoghue P.C.J. Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils.Palaeontology. 2015; 58: 769-785Crossref PubMed Scopus (137) Google Scholar, 5Blank C.E. Sánchez-Baracaldo P. Timing of morphological and ecological innovations in the cyanobacteria--a key to understanding the rise in atmospheric oxygen.Geobiology. 2010; 8: 1-23Crossref PubMed Scopus (183) Google Scholar, 6Sánchez-Baracaldo P. Ridgwell A. Raven J.A. A neoproterozoic transition in the marine nitrogen cycle.Curr. Biol. 2014; 24: 652-657Abstract Full Text Full Text PDF PubMed Scopus (83) Google Scholar, 7Schirrmeister B.E. de Vos J.M. Antonelli A. Bagheri H.C. Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event.Proc. Natl. Acad. Sci. USA. 2013; 110: 1791-1796Crossref PubMed Scopus (213) Google Scholar, 8Sánchez-Baracaldo P. Origin of marine planktonic cyanobacteria.Sci. Rep. 2015; 5: 17418Crossref PubMed Scopus (102) Google Scholar, 9Sánchez-Baracaldo P. Raven J.A. Pisani D. Knoll A.H. Early photosynthetic eukaryotes inhabited low-salinity habitats.Proc. Natl. Acad. Sci. USA. 2017; 114: E7737-E7745Crossref PubMed Scopus (166) Google Scholar] to ∼500 Ma [10Shih P.M. Hemp J. Ward L.M. Matzke N.J. Fischer W.W. Crown group Oxyphotobacteria postdate the rise of oxygen.Geobiology. 2017; 15: 19-29Crossref PubMed Scopus (104) Google Scholar]. The older estimates are invariably calibrated by putative akinete fossils from Paleoproterozoic-Mesoproterozoic rocks around 2,100–1,400 Ma [3Tomitani A. Knoll A.H. Cavanaugh C.M. Ohno T. The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives.Proc. Natl. Acad. Sci. USA. 2006; 103: 5442-5447Crossref PubMed Scopus (338) Google Scholar, 11Golubic S. Sergeev V.N. Knoll A.H. Mesoproterozoic Archaeoellipsoides: akinetes of heterocystous cyanobacteria.Lethaia. 1995; 28: 285-298Crossref PubMed Scopus (92) Google Scholar, 12Amard B. Bertrand-Sarfati J. Microfossils in 2000 Ma old cherty stromatolites of the Franceville Group, Gabon.Precambrian Res. 1997; 81: 197-221Crossref Google Scholar]. However, the interpretation of these fossils as akinetes has been questioned [13Butterfield N.J. Proterozoic photosynthesis – a critical review.Palaeontol. 2015; 58: 953-972Crossref Scopus (79) Google Scholar], and the next oldest akinete and heterocyst fossils are ∼410 Ma [14Croft W.N. George E.A. Blue-green algae from the Middle Devonian of Rhynie, Aberdeenshire. Bull. Br. Mus. (Nat. Hist.).Geol. Ser. 1959; 3: 341-353Google Scholar]. Thus, the scarcity of reliable heterocystous cyanobacterial fossils significantly hampers our understanding of the evolution of complex multicellularity among cyanobacteria, their role in regulating geochemical cycles in the geological past, and our ability to calibrate cyanobacterial molecular clocks. Here, we report Tonian (∼1,000–720 Ma) filamentous cyanobacteria that are characterized by large cells, binary fission (for filament elongation), hormogonia (for asexual reproduction and dispersal), probable akinetes (for survival in adverse conditions), and by implication, diazotrophic heterocysts. The new fossils provide a minimum age calibration on the divergence of subsections IV+V and place a firm constraint on the evolution of akinetes and heterocysts. Cyanobacteria were the ultimate ancestor of all plastids and, for much of Earth’s history, the only source of biogenic oxygen and a major source of fixed carbon and nitrogen. One cyanobacterial clade, subsections IV+V, is characterized by multicellularity and cell differentiation, with many members bearing specialized nitrogen-fixing (or diazotrophic) heterocysts and encysting akinetes [1Adams D.G. Duggan P.S. Heterocyst and akinete differentiation in cyanobacteria.New Phytol. 1999; 144: 3-33Crossref Scopus (194) Google Scholar, 2Castenholz R.W. Cyanobacteria: oxygenic photosynthetic bacteria.in: Boone D.R. Castenholz R.W. Garrity G.M. Bergey’s Manual of Systematic Bacteriology. Second Edition. Volume 1. Springer, New York2001: 473-599Crossref Google Scholar, 3Tomitani A. Knoll A.H. Cavanaugh C.M. Ohno T. The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives.Proc. Natl. Acad. Sci. USA. 2006; 103: 5442-5447Crossref PubMed Scopus (338) Google Scholar]. Molecular clock estimates of the divergence time of this clade are highly variable, ranging from ∼2,000 Ma (mega-annum) [4Schirrmeister B.E. Gugger M. Donoghue P.C.J. Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils.Palaeontology. 2015; 58: 769-785Crossref PubMed Scopus (137) Google Scholar, 5Blank C.E. Sánchez-Baracaldo P. Timing of morphological and ecological innovations in the cyanobacteria--a key to understanding the rise in atmospheric oxygen.Geobiology. 2010; 8: 1-23Crossref PubMed Scopus (183) Google Scholar, 6Sánchez-Baracaldo P. Ridgwell A. Raven J.A. A neoproterozoic transition in the marine nitrogen cycle.Curr. Biol. 2014; 24: 652-657Abstract Full Text Full Text PDF PubMed Scopus (83) Google Scholar, 7Schirrmeister B.E. de Vos J.M. Antonelli A. Bagheri H.C. Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event.Proc. Natl. Acad. Sci. USA. 2013; 110: 1791-1796Crossref PubMed Scopus (213) Google Scholar, 8Sánchez-Baracaldo P. Origin of marine planktonic cyanobacteria.Sci. Rep. 2015; 5: 17418Crossref PubMed Scopus (102) Google Scholar, 9Sánchez-Baracaldo P. Raven J.A. Pisani D. Knoll A.H. Early photosynthetic eukaryotes inhabited low-salinity habitats.Proc. Natl. Acad. Sci. USA. 2017; 114: E7737-E7745Crossref PubMed Scopus (166) Google Scholar] to ∼500 Ma [10Shih P.M. Hemp J. Ward L.M. Matzke N.J. Fischer W.W. Crown group Oxyphotobacteria postdate the rise of oxygen.Geobiology. 2017; 15: 19-29Crossref PubMed Scopus (104) Google Scholar]. The older estimates are invariably calibrated by putative akinete fossils from Paleoproterozoic-Mesoproterozoic rocks around 2,100–1,400 Ma [3Tomitani A. Knoll A.H. Cavanaugh C.M. Ohno T. The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives.Proc. Natl. Acad. Sci. USA. 2006; 103: 5442-5447Crossref PubMed Scopus (338) Google Scholar, 11Golubic S. Sergeev V.N. Knoll A.H. Mesoproterozoic Archaeoellipsoides: akinetes of heterocystous cyanobacteria.Lethaia. 1995; 28: 285-298Crossref PubMed Scopus (92) Google Scholar, 12Amard B. Bertrand-Sarfati J. Microfossils in 2000 Ma old cherty stromatolites of the Franceville Group, Gabon.Precambrian Res. 1997; 81: 197-221Crossref Google Scholar]. However, the interpretation of these fossils as akinetes has been questioned [13Butterfield N.J. Proterozoic photosynthesis – a critical review.Palaeontol. 2015; 58: 953-972Crossref Scopus (79) Google Scholar], and the next oldest akinete and heterocyst fossils are ∼410 Ma [14Croft W.N. George E.A. Blue-green algae from the Middle Devonian of Rhynie, Aberdeenshire. Bull. Br. Mus. (Nat. Hist.).Geol. Ser. 1959; 3: 341-353Google Scholar]. Thus, the scarcity of reliable heterocystous cyanobacterial fossils significantly hampers our understanding of the evolution of complex multicellularity among cyanobacteria, their role in regulating geochemical cycles in the geological past, and our ability to calibrate cyanobacterial molecular clocks. Here, we report Tonian (∼1,000–720 Ma) filamentous cyanobacteria that are characterized by large cells, binary fission (for filament elongation), hormogonia (for asexual reproduction and dispersal), probable akinetes (for survival in adverse conditions), and by implication, diazotrophic heterocysts. The new fossils provide a minimum age calibration on the divergence of subsections IV+V and place a firm constraint on the evolution of akinetes and heterocysts. The fossils were collected from the Tonian (∼1,000–720 Ma) Liulaobei Formation in the Huainan region of North China (Figure S1) and are described as Anhuithrix magna new genus and new combination (Figures 1, 2, and 3A–3F ; see Data S1 for systematic description). They are uniserial filaments occurring as aggregates with other filamentous fossils to form microbial mats (Figures 1A, 1B, and 1E) or as isolated individuals (Figures 1C and 1H–1K). When preserved as aggregates, filaments seem to be embedded in a common mucilaginous matrix as represented by the faint amorphous organic matter surrounding the aggregates (white arrowheads in Figure 1A). When preserved in isolation, trichomes may be enveloped by a thin and non-lamellated extracellular sheath as indicated by the faint organic membranes enveloping loosely concatenated cells (arrowheads in Figure 1H). Individual filaments can be straight, curved, bent, or twisted (Figures 1C, 1E, 1J, and 1K), with a diameter of 141–615 μm (mean = 359 μm; SD = 81 μm; n = 330; Figure 4B) and a length up to 2 cm. Trichomes each consist of 3–140 cells, with 3–14 cells per mm length. Some trichomes show evidence of fragmentation (Figure 2A), resulting in shorter trichomes with rounded terminal cells (Figure 2B). Cells can be tightly arranged with narrow gaps in between (Figures 1G and 1K) or loosely concatenated with notable gaps (Figures 1D and 1I). Individual cells occasionally deviate from linear alignment (arrows in Figure 1K), perhaps due to taphonomic dislocation. Apical cells are globose (Figures 1F, 2B, 2D, and 3D), hemispherical (Figure 2A), obtusely rounded (Figure 3A), or conical (Figure 1C). Medial cells are discoidal (Figures 1G, 1H, and 1J) to isodiametric (Figure 1D) in shape, sometimes with constrictions at cell boundaries or septa (Figure 1K). The discoidal nature of the medial cells can be appreciated in obliquely compressed cells, where lateral cell walls are darker or better preserved than transverse septa (Figures 1H and 2G). Cells are relatively large, 56–425 μm in length (mean = 173 μm; SD = 55 μm; n = 1,602) and 113–614 μm in width (mean = 304 μm; SD = 73 μm; n = 1,602), with cell length/width ratios mostly ≤1 (Figure 4A). Paired cells are occasionally present (Figure 2A); these cells are typically 0.5–1× the length of neighboring un-paired ones, so that the lengths of the longest and shortest cells in the same trichome are plotted mostly between the 2:1 and 1:1 lines (Figure 4C). What distinguishes A. magna from other filamentous fossils is the sparse presence of distinctively large globose cells, 364–800 μm in diameter (mean = 492 μm; SD = 163 μm; n = 6), that can be present terminally (Figures 1F, 2D, and 3D) or medially (Figures 2C, 2E, and 2F).Figure 2Hormogonia, Paired Cells, and Akinetes of A. magnaShow full caption(A) Trichome in the process of fragmentation to form hormogonia. Note hemispherical and terminally rounded apical cells (arrowheads, indicating that fragmentation was biological, not taphonomic) and cell pairs (arrow, suggesting binary fission); PB21747.(B) Short trichome consisting of three cells; PB21748.(C–F) Trichomes with large globose cells interpreted as akinetes (arrows); (C) PB21749; (D) PB21750; (E) PB21751; (F) PB21752.(G) Trichome with “hollow” cells (arrows) of obliquely compressed cells with poor preservation of septa (also see Figure 1H). Note fragmentation with broken terminal cells (arrowheads), probably due to post-mortem disintegration; PB21753.Scale bars, 500 μm ([A], [C], and [E]–[G]) and 200 μm ([B] and [D]). See also Table S1 and Data S1.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Figure 3Preservation of A. magna and Co-existing Carbonaceous FossilsShow full captionReflected-light microscopic images ([A], [D], and [G]–[I]), BSE-SEM images ([B] and [E]), and EDS elemental maps ([C] and [F]).(A–C) Fragments of A. magna with obtusely rounded apical cell (arrow in [A]). (B) BSE-SEM image; ([C1]–[C9]) are C, O, Si, Al, Fe, S, Ca, Mg, and K maps of rectangle in (A); PB21754.(D–F) Trichome of A. magna with large globose cell interpreted as akinete (arrow in [D]). (E) BSE-SEM image; ([F1]–[F9]) are C, O, Si, Al, Fe, S, Ca, Mg, and K maps of rectangle in (D); PB21755.(G and H) Filaments of Mucoplagum primitivum. Note the densely packed aggregates in (H); (G) PB21756; (H) PB21757.(I) Siphonophycus gigas; PB21758.Scale bars, 1 mm ([D] and [G]–[I]) and 500 μm ([A]–[C], [E], and [F]). See also Data S1. BSE-SEM, backscattered scanning electron microscopy; EDS, energy dispersive X-ray spectroscopy.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Figure 4Biometric Analysis of A. magnaShow full caption(A) Cross-plot and frequency distribution of cell width (W) and length (L). Most cells (97.6%; 1,563 out of 1,602 measured cells) have length:width ratios ≤1.(B) Frequency distribution of filament diameter (measured at the widest point of a filament).(C) Cross-plot of shortest (Ls) and longest (Ll) cell length in the same filament. Most measurements of Ll/Ls length ratios (mean = 1.58) is within the expected range of 1.00–2.00.See Tables S1 and S2 for cell size measurements of living and fossil cyanobacteria, sulfur-oxidizing bacteria, and green algae.View Large Image Figure ViewerDownload Hi-res image Download (PPT) (A) Trichome in the process of fragmentation to form hormogonia. Note hemispherical and terminally rounded apical cells (arrowheads, indicating that fragmentation was biological, not taphonomic) and cell pairs (arrow, suggesting binary fission); PB21747. (B) Short trichome consisting of three cells; PB21748. (C–F) Trichomes with large globose cells interpreted as akinetes (arrows); (C) PB21749; (D) PB21750; (E) PB21751; (F) PB21752. (G) Trichome with “hollow” cells (arrows) of obliquely compressed cells with poor preservation of septa (also see Figure 1H). Note fragmentation with broken terminal cells (arrowheads), probably due to post-mortem disintegration; PB21753. Scale bars, 500 μm ([A], [C], and [E]–[G]) and 200 μm ([B] and [D]). See also Table S1 and Data S1. Reflected-light microscopic images ([A], [D], and [G]–[I]), BSE-SEM images ([B] and [E]), and EDS elemental maps ([C] and [F]). (A–C) Fragments of A. magna with obtusely rounded apical cell (arrow in [A]). (B) BSE-SEM image; ([C1]–[C9]) are C, O, Si, Al, Fe, S, Ca, Mg, and K maps of rectangle in (A); PB21754. (D–F) Trichome of A. magna with large globose cell interpreted as akinete (arrow in [D]). (E) BSE-SEM image; ([F1]–[F9]) are C, O, Si, Al, Fe, S, Ca, Mg, and K maps of rectangle in (D); PB21755. (G and H) Filaments of Mucoplagum primitivum. Note the densely packed aggregates in (H); (G) PB21756; (H) PB21757. (I) Siphonophycus gigas; PB21758. Scale bars, 1 mm ([D] and [G]–[I]) and 500 μm ([A]–[C], [E], and [F]). See also Data S1. BSE-SEM, backscattered scanning electron microscopy; EDS, energy dispersive X-ray spectroscopy. (A) Cross-plot and frequency distribution of cell width (W) and length (L). Most cells (97.6%; 1,563 out of 1,602 measured cells) have length:width ratios ≤1. (B) Frequency distribution of filament diameter (measured at the widest point of a filament). (C) Cross-plot of shortest (Ls) and longest (Ll) cell length in the same filament. Most measurements of Ll/Ls length ratios (mean = 1.58) is within the expected range of 1.00–2.00. See Tables S1 and S2 for cell size measurements of living and fossil cyanobacteria, sulfur-oxidizing bacteria, and green algae. A. magna is preserved as carbonaceous compressions (Figures 3B and 3E; see Supplemental Information for discussion on preservation). Some aspects of A. magna morphology were probably derived from taphonomic alteration. For example, cell dislocation from linear alignment (Figure 1K) may be due to tearing or shearing, and cell shrinkage (Figures 1I and 2G) and cell separation with notable gaps (Figures 1D and 1I) may be due to degradation. Similar taphonomic modifications have been routinely observed in taphonomic experiments and cyanobacterial fossils [15Golubic S. Barghoorn E.S. Interpretation of microbial fossils with special reference to the Precambrian.in: Flügel E. Fossil Algae: Recent Results and Developments. Springer-Verlag, Berlin1977: 1-14Crossref Google Scholar, 16Oehler J.H. Experimental studies in Precambrian paleontology: Structural and chemical changes in blue-green algae during simulated fossilization in synthetic chert.Geol. Soc. Am. Bull. 1976; 87: 117-129Crossref Scopus (84) Google Scholar]. However, cell pairs (Figure 2A), large globose cells occurring terminally or medially (Figures 1F, 2C–2F, and 3D), and hemispherical or terminally rounded apical cells (Figures 2A, 2B, and 3A) are regarded as biological features because of their stable shape and consistent occurrence. As such, short trichomes with rounded terminal cells (Figure 2B) likely represent biological fragmentation, as opposed to taphonomic artifacts where cell dislocation, rotation, shrinkage, and breakage would occur (Figure 2G). Cell pairs in A. magna are interpreted as evidence for transverse binary fission, a process of cell division in the plane perpendicular to trichome length, and a growth mechanism in filamentous bacteria (e.g., the extant cyanobacterium Johannesbaptistia) and eukaryotes [2Castenholz R.W. Cyanobacteria: oxygenic photosynthetic bacteria.in: Boone D.R. Castenholz R.W. Garrity G.M. Bergey’s Manual of Systematic Bacteriology. Second Edition. Volume 1. Springer, New York2001: 473-599Crossref Google Scholar, 17Enzien M.V. Cyanobacteria or rhodophyta? Interpretation of a precambrian microfossil.Biosystems. 1990; 24: 245-251Crossref PubMed Scopus (4) Google Scholar]. Cell shrinkage sometimes can produce spool-shaped bodies in filamentous cyanobacteria [15Golubic S. Barghoorn E.S. Interpretation of microbial fossils with special reference to the Precambrian.in: Flügel E. Fossil Algae: Recent Results and Developments. Springer-Verlag, Berlin1977: 1-14Crossref Google Scholar], superficially resembling cell pairs after cell division. However, cell pairs in A. magna are morphologically consistent and do not show evidence of stronger shrinkage than neighboring cells; thus, they likely represent cell division rather than taphonomic shrinkage. Cell pairs in A. magna are different from the Mesoproterozoic red alga Bangiomorpha, where cell pairs are hierarchically nested [18Butterfield N.J. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes.Paleobiology. 2000; 26: 386-404Crossref Scopus (507) Google Scholar]. Instead, they are broadly similar to binary fission in cyanobacteria [17Enzien M.V. Cyanobacteria or rhodophyta? Interpretation of a precambrian microfossil.Biosystems. 1990; 24: 245-251Crossref PubMed Scopus (4) Google Scholar]. This interpretation is also consistent with morphometric data showing that length ratios of the longest to shortest cells in the same trichome are mostly within the range of 1.0–2.0 (Figure 4C); as binary fission tends to halve the cell length in each cell division, the ratios are expected to be in the range of 1.0–2.0 considering growth after each cell division. Short trichomes with hemispherical or terminally rounded apical cells are interpreted as hormogonia, which are short and motile segments of trichomes for asexual reproduction and dispersal purposes. Their apical cells are similar to those in hormogonia of modern filamentous cyanobacteria (e.g., Figure 1.16 of reference [19Tappan H.N. The Paleobiology of Plant Protists. W.H. Freeman and Company, San Francisco1980Google Scholar]) but different from deflated, broken, rotated, or dislocated terminal cells in fragments produced by post-mortem disintegration (Figure 2G). Short trichomes of A. magna consist of 3–10 cells, similar to modern cyanobacterial hormogonia, which typically have <15 cells [2Castenholz R.W. Cyanobacteria: oxygenic photosynthetic bacteria.in: Boone D.R. Castenholz R.W. Garrity G.M. Bergey’s Manual of Systematic Bacteriology. Second Edition. Volume 1. Springer, New York2001: 473-599Crossref Google Scholar]. Large globose cells in A. magna are interpreted as resting cells akin to akinetes in subsections IV+V of modern cyanobacteria [1Adams D.G. Duggan P.S. Heterocyst and akinete differentiation in cyanobacteria.New Phytol. 1999; 144: 3-33Crossref Scopus (194) Google Scholar]. Akinetes are typically distinguished from vegetative cells by their relatively large size, an envelope enriched in less water-soluble polysaccharides, and a thicker cell wall [11Golubic S. Sergeev V.N. Knoll A.H. Mesoproterozoic Archaeoellipsoides: akinetes of heterocystous cyanobacteria.Lethaia. 1995; 28: 285-298Crossref PubMed Scopus (92) Google Scholar, 20Herdman M. Akinetes: structure and function.in: Fay P. Baalen C.V. The Cyanobacteria. Elsevier, Amsterdam1987: 227-250Google Scholar]. These features enable akinetes to survive adverse conditions and enhance their fossilization potential [11Golubic S. Sergeev V.N. Knoll A.H. Mesoproterozoic Archaeoellipsoides: akinetes of heterocystous cyanobacteria.Lethaia. 1995; 28: 285-298Crossref PubMed Scopus (92) Google Scholar, 20Herdman M. Akinetes: structure and function.in: Fay P. Baalen C.V. The Cyanobacteria. Elsevier, Amsterdam1987: 227-250Google Scholar]. Although heterocysts are also larger and thicker walled than vegetative cells, they tend to be regularly spaced (e.g., interspersed by 10–20 vegetative cells in Anabaena [2Castenholz R.W. Cyanobacteria: oxygenic photosynthetic bacteria.in: Boone D.R. Castenholz R.W. Garrity G.M. Bergey’s Manual of Systematic Bacteriology. Second Edition. Volume 1. Springer, New York2001: 473-599Crossref Google Scholar]). Because of their irregular occurrence in the trichomes, the large globose cells in A. magna are interpreted as akinetes rather than heterocysts. Because molecular phylogenetic data strongly suggest that akinete-bearing cyanobacteria are nested within a clade of heterocystous cyanobacteria (Figure S7 of reference [21Uyeda J.C. Harmon L.J. Blank C.E. A comprehensive study of cyanobacterial morphological and ecological evolutionary dynamics through deep geologic time.PLoS ONE. 2016; 11: e0162539Crossref PubMed Scopus (44) Google Scholar]) and also because modern akinetes occur almost exclusively in heterocystous cyanobacteria but the reverse is not true (Table S1), akinetes likely arose within heterocystous cyanobacteria, the origin of akinetes post-dates that of heterocysts, and akinetes are a robust proxy for heterocysts although the reverse is untrue. Thus, the presence of akinetes alludes to the possibility that A. magna is a heterocystous cyanobacterium (i.e., a member of subsections IV+V). A cyanobacterium affinity for A. magna is additionally supported by the better preservation of the lateral cell walls relative to the septa, a feature best seen in obliquely compressed cells (Figures 1H and 2G) and often observed in other Precambrian cyanobacterial trichomes [22Schopf J.W. Kudryavtsev A.B. Tripathi A.B. Czaja A.D. Three-dimensional morphological (CLSM) and chemical (Raman) imagery of cellularly mineralized fossils.in: Allison P.A. Bottjer D.J. Taphonomy: Process and Bias Through Time. Second Edition. Volume 32. Springer, New York2011: 457-486Google Scholar]. This differential preservation can be explained by the different structure and biochemistry between the lateral cell walls and septa of cyanobacterial trichomes [23Drews G. Fine structure and chemical composition of the cell envelopes.in: Carr N.G. Whitton B.A. The Biology of Blue-Green Algae. Volume 9. University of California Press, Berkeley1973: 99-116Google Scholar]. The lateral cell walls of modern cyanobacterial trichomes typically consist of four layers, including two outer layers (L3 and L4) and two inner layers (L1 and L2, although L1 may be an artifact). Septum formation is initiated during cell division through centripetal ingrowth of the cytoplasmic membrane and layers L1–L2. Thus, septa only consist of layers L1–L2 and lack layers L3–L4 [23Drews G. Fine structure and chemical composition of the cell envelopes.in: Carr N.G. Whitton B.A. The Biology of Blue-Green Algae. Volume 9. University of California Press, Berkeley1973: 99-116Google Scholar, 24Ris H. Singh R.N. Electron microscope studies on blue-green algae.J. Biophys. Biochem. Cytol. 1961; 9: 63-80Crossref PubMed Scopus (65) Google Scholar]. Moreover, the synthesis of peptidoglycan, an essential component rigidifying cyanobacterial cell walls, ceases after an initial centripetal growth of layer L2, thus only the peripheral portion of the septa is rich in peptidoglycan [22Schopf J.W. Kudryavtsev A.B. Tripathi A.B. Czaja A.D. Three-dimensional morphological (CLSM) and chemical (Raman) imagery of cellularly mineralized fossils.in: Allison P.A. Bottjer D.J. Taphonomy: Process and Bias Through Time. Second Edition. Volume 32. Springer, New York2011: 457-486Google Scholar, 23Drews G. Fine structure and chemical composition of the cell envelopes.in: Carr N.G. Whitton B.A. The Biology of Blue-Green Algae. Volume 9. University of California Press, Berkeley1973: 99-116Google Scholar]. The combined result is that septa are relatively thin and deficient in peptidoglycan in comparison with lateral walls, accounting for the differential preservation observed in A. magna and other filamentous cyanobacterial fossils [22Schopf J.W. Kudryavtsev A.B. Tripathi A.B. Czaja A.D. Three-dimensional morphological (CLSM) and chemical (Raman) imagery of cellularly mineralized fossils.in: Allison P.A. Bottjer D.J. Taphonomy: Process and Bias Through Time. Second Edition. Volume 32. Springer, New York2011: 457-486Google Scholar]. It should be pointed out that, although a peptidoglycan layer forms the septum in some gram-negative bacteria such as the sulfur-oxidizing bacteria Beggiatoa [25Strohl W.R. Larkin J.M. Cell division and trichome breakage inBeggiatoa.Curr. Microbiol. 1978; 1: 151-155Crossref PubMed Scopus (11) Google Scholar], such a structural difference between the lateral and cross walls is not typical of filamentous eukaryotic algae [26Dodge J.D. The Fine Structure of Algal Cells. Academic Press, London1973Google Scholar], which together with other morphological features suggests that A. magna is unlikely a eukaryote. Filaments of A. magna often occur as a main structural element in densely packed aggregates of filaments, where they are intertwined with each other and with other filamentous taxa such as Mucoplagum primitivum, Siphonophycus solidum, S. puntatum, and S. gigas (Figures 1A and 3G–3I). Amorphous carbonaceous material surrounding the aggregates is interpreted as extracellular polymeric substance (EPS). Similarly, amorphous carbonaceous material surrounding filaments is interpreted as mucilaginous sheath. Thus, A. magna was likely a benthic microbial mat builder. A. magna is noted for its large cell size. Its akinetes and vegetative cells are larger than those of modern and fossil filamentous cyanobacteria (Tables S1 and S2), although a few modern cyanobacteria (e.g., Lyngbya majuscula and Oscillatoria princeps) and filamentous fossils interpreted by some as cyanobacteria (e.g., Rugosoopsis rugososiusculus, Grypania spiralis, and Katnia singhii) do have comparable or even larger cell sizes. Cell size has traditionally played a central role in the phylogenetic interpretation of microfossils [27Schopf J.W. Proterozoic prokaryotes: Affinities, geologic distribution, and evolutionary trends.in: Schopf J.W. Klein C. The Proterozoic Biosphere: A Multidisciplinary Study. Cambridge University Press, New York1992: 195-218Crossref Google Scholar], but the significant overlap in cell-size range between bacteria and eukaryotes (Table S2) [27Schopf J.W. Proterozoic prokaryotes: Affinities, geologic distribution, and evolutionary tre" @default.
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