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Glaphyrobalantium hueberi gen. et sp. nov., a Cryptic Microbial Fossil,

Presumably a Cyanobacterium or Microscopic Alga, from the Lower Devonian
Rhynie Chert

Article in International Journal of Plant Sciences · May 2022

DOI: 10.1086/720386

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 SPECIAL ISSUE—TRIBUTE TO FRANCIS M. HUEBER

GLAPHYROBALANTIUM HUEBERI GEN. ET SP. NOV., A CRYPTIC MICROBIAL FOSSIL,

PRESUMABLY A CYANOBACTERIUM OR MICROSCOPIC ALGA, FROM THE
LOWER DEVONIAN RHYNIE CHERT
Michael Krings1,*

*SNSB–Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Strasse 10, 80333 Munich, Germany; Department of Earth
and Environmental Sciences, Paleontology, and Geobiology, Ludwig-Maximilians-Universität München, Richard-Wagner-Strasse 10,
80333 Munich, Germany; and Department of Ecology and Evolutionary Biology and Natural History Museum and Biodiversity
Institute, University of Kansas, Lawrence, Kansas 66045-7534, USA

Guest Editor: Kelly Matsunaga

Premise of research. The Lower Devonian Rhynie chert preserves abundant microbial fossils that are similar
morphologically to cyanobacteria and microscopic algae but cannot be placed systematically with confidence.
Although often morphologically distinct, only a few of these fossils have been described.
Methodology. Thin sections prepared from three different blocks of the Rhynie chert were examined at high
magnification in transmitted light. Images of fossils were captured digitally and processed in Adobe Photoshop.
Pivotal results. More than 150 specimens of Glaphyrobalantium hueberi gen. et sp. nov., a minute vesicle bounded
by a prominent envelope and usually containing eight or more spherical bodies, were found. The fossils are similar
to certain present-day coccoid cyanobacteria (e.g., Gloeocapsa; Chroococcales) and algae (e.g., Gloeocystis;
Sphaeropleales) that occur in microscopic groups of two to eight (or more) cells surrounded by a colonial sheath
and unicellular algae that reproduce asexually by autospores (e.g., Chlorococcum; Chlamydomonadales), but affin-
ities to protists, fungi, and fungus-like organisms can also not be ruled out.
Conclusions. This discovery expands our knowledge of microbial life in the Rhynie paleoecosystem. Although
the affinities remain elusive, it is important to describe fossils like G. hueberi as a first step toward understanding
past microbial biodiversity and the roles microorganisms have had as constituents of ancient ecosystems.

Keywords: autospores, biodiversity, Chlorophyta, colonial sheath, Gloeocapsa, multicellularity.

Introduction Cyanobacteria and microscopic algae (microalgae) probably

were taxonomically diverse and occurred in large quantities in
The Lower Devonian Rhynie chert of Scotland has attracted the Rhynie paleoecosystem. However, relatively few of these life
attention primarily because it contains exquisite fossils of early forms have been documented in detail and formally described
land plants that have substantially advanced our perception of (e.g., Croft and George 1959; Edwards and Lyon 1983; Dotzler
the early evolution of vascular plant life on land (Taylor et al. et al. 2007; Krings et al. 2007, 2017b, 2017c; Krings 2019,
2005; Kerp 2017). Equally important has been the documenta- 2021b, 2021c), in part because the classification of cyanobac-
tion of animal life from the Rhynie chert (Anderson and Trewin teria and microalgae today largely relies on molecular sequenc-
2003; Dunlop and Garwood 2017). Moreover, the earliest ing and features that are difficult, if not impossible, to obtain
scholars studying the plants also documented various types of from fossils (Komárek et al. 2014; Heimann and Huerlimann
microorganisms, especially fungi (Kidston and Lang 1921). Al- 2015; Wilmotte et al. 2017; Xu et al. 2020). As a result, many
though a long hiatus exists between this pioneering work and microbial fossils that might be cyanobacteria or microalgae can-
subsequent reports on microbial life, there has been a continu- not be placed systematically through comparison with modern
ously growing interest in the microbial component of the Rhynie analogues. Nevertheless, some of these fossils display structural
chert biota during the past 30 years (Krings et al. 2017a; Trewin features that, albeit not necessarily diagnostic, are consistent
and Kerp 2017; Garwood et al. 2020). among specimens and thus make it possible to recognize distinc-
tiveness. Hence, a first step toward understanding these organ-
isms in the Rhynie paleoecosystem is to report the occurrence
1
Email: [email protected]. of morphologies with a high recognition value and document
Manuscript received October 2021; revised manuscript received December 2021; them as thoroughly as possible (Taylor and Krings 2015; Krings
electronically published May 11, 2022. et al. 2017b, 2017c).

International Journal of Plant Sciences, volume 183, number 6, July/August 2022. q 2022 The University of Chicago. All rights reserved. Published
by The University of Chicago Press. https://doi.org/10.1086/720386

432
 KRINGS—A CRYPTIC RHYNIE CHERT MICROBIAL FOSSIL 433

This study describes an unusual microbial fossil from the of 2–10(–30) in the chert matrix, within loose or compacted
Rhynie chert that is relatively common in places and typically accumulations of fragmented and partially to largely degraded
occurs in the chert matrix. Specimens are spheroidal, ovoid, or land plant remains, coccoid and filamentous cyanobacteria, var-
irregularly shaped vesicles that usually contain eight or more ious types of fungal hyphae and reproductive units, scattered
spherical bodies. They are similar morphologically to certain remnants of arthropod exuviae, land plant spores, unidentifiable
present-day chroococcalean cyanobacteria and microscopic al- organic matter, and varying amounts of sediment (fig. 1A). Most
gae, but affinities to protists, fungi, and fungus-like organisms of the specimens in block 2016 XII are closely associated with a
can also not be ruled out. Scytonema-like filamentous cyanobacterium that grows in dense
tangles on surfaces and within the peripheral tissue layers of
Geological Setting decaying land plant parts (fig. 1B, 1C). Specimens are sometimes
also located in voids in plant material; however, they seem to
The Rhynie chert Lagerstätte (comprising the Rhynie and have been washed into these spaces rather than developed within
Windyfield chert sites) is located in the northern part of the the plants. The abundance of cyanobacteria in the sections sug-
Rhynie outlier of Lower Old Red Sandstone in Aberdeenshire, gests that the contexts represent plant litter layers within a wet
Scotland, in an extensive sequence of sedimentary and volcanic or aquatic facies. Specimens in block SNSB-BSPG 2008 XVI are
rocks. The chert occurs in the Rhynie Block of the Dryden Flags located in a microbial mat dominated by Croftalania venusta,
Formation located northwest of the village of Rhynie. The Lager- a filamentous putative cyanobacterium that was a common mi-
stätte is made up of fossiliferous beds containing lacustrine shales crobial mat framework builder in the Rhynie paleoecosystem
and chert that have been interpreted as ephemeral pools within (Krings et al. 2007; Krings 2021a). All fossils are preserved as
a geothermal wetland (Channing 2017; Trewin and Kerp 2017), three-dimensional petrifactions.
with alkali-chloride hot springs that were part of a complex hydro- Specimens (figs. 1D–1H, 2) are spheroidal, prolate spheroidal,
thermal system in a region affected by volcanic activity (Rice et al. ovoid, pyriform, somewhat elongated (cylindrical), or, rarely, ir-
2002; Rice and Ashcroft 2004; Trewin and Fayers 2016). Pre- regular or asymmetrical in shape, and they are between 25 and
served in the chert are both aquatic facies from the pools and ca. 40 mm in diameter, or 35–55 mm long and up to 35(–40) mm
subaerial soil/litter horizons with in situ plants that grew along wide and high. They typically consist of three component parts,
the margins of the pools; preservation is thought to have taken for which henceforth the informal denotations “vesicle” (v in
place as a result of temporary flooding of silica-rich water or fig. 1H), “envelope” (e in fig. 1H), and “bodies” (b in fig. 1H)
by groundwater high in silica percolating to the surface (Powell are used. However, there are also scattered specimens that lack
et al. 2000). The Rhynie chert biota is regarded as 411.5 5 1.3 recognizable bodies but instead either are empty or contain amor-
to 407.6 5 2.6 Myr old according to Mark et al. (2011) and phous black or brownish matter (arrows in fig. 1D). Still other
Parry et al. (2011) and Pragian to earliest Emsian according to specimens occur in the form of hollow spaces shaped like the fos-
Wellman (2006, 2017) and Wellman et al. (2006). For details sil that are filled with abundant black matter (arrow in fig. 1G).
on the geology and paleontology of the Rhynie chert, refer to As to whether these specimens represent (advanced) states of nat-
Trewin and Kerp (2017), Garwood et al. (2020), and the volume ural decay or artifacts of silicification, or both, remains unresolved.
edited by Edwards et al. (2018). The vesicle is a simple cavity bounded on the outside by a dark
boundary line up to 0.5 mm thick. The boundary line is typically
Material and Methods smooth but may rarely also be distorted or irregularly wrinkled
(arrow in fig. 1E). Surrounding the vesicle is a prominent, color-
Specimens were identified in series of thin sections prepared less, translucent, and unstratified envelope, which may vary in
from three Rhynie chert blocks by cementing wafers of the rocks thickness from less than 1 to 4.5(–5) mm, both within and be-
to glass slides and then grinding the slices until they were suf- tween individuals; it is bounded on the outside by a delicate limit,
ficiently thin to transmit light. All materials are deposited in the which occurs in the form of a dark line less than 0.5 mm thick.
Bayerische Staatssammlung für Paläontologie und Geologie (SNSB- The outer surface is smooth in most specimens but may some-
BSPG) at Munich, Germany, under accession numbers SNSB- times show local ruptures of the limit line. A few specimens sug-
BSPG 2008 XVI 1–45, 2015 XVII 1–23, and 2016 XII 1–42. gest that there was a surface ornamentation composed of fine
For comparison, specimens of other Rhynie chert microfossils reticulations (fig. 2O5); however, this feature could also be a
from the holdings of the SNSB-BSPG have also been illustrated. preservation artifact that resulted from shrinkage of the struc-
All fossils were examined using normal transmitted light micros- tures during fossilization. There are also a few specimens (fewer
copy; images were captured with a Leica DFC-480 digital camera than 10) in which the envelope is partially missing (fig. 2I) and
and processed for brightness and contrast in Adobe Photoshop others (fewer than 5) that show one or several papilla-like pro-
CS5 (for details on microscopy and image optimization, refer to trusions of the envelope (fig. 2N1). Several of the specimens sug-
Krings et al. 2021). Slide numbers for the specimens illustrated gest that the entire structure was additionally surrounded by
are included in the figure legends. diffluent, colorless mucilage (arrow in fig. 2D).
Vesicles usually contain eight (see fig. 2H1–3) or more (up to 30
Results have been counted in several specimens; e.g., fig. 2O, 2P) bodies,
which are generally spherical or spheroidal in outline, but some
More than 150 well-preserved specimens of the fossils de- may also be deformed due to space constraints or irregularly
scribed below have been discovered from the thin sections pre- wrinkled (fig. 2N1) and 6.5–10 mm in diameter. Vesicles contain-
pared from the three chert blocks. Specimens in blocks SNSB- ing two or four bodies have also been encountered but appear to
BSPG 2015 XVII and 2016 XII occur singly or in small groups be generally rare. The bodies all are bounded on the outside by a
434 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 1 Context and morphology of Glaphyrobalantium hueberi from the Lower Devonian Rhynie chert. A, Portion of a thin section prepared
from block SNSB-BSPG 2016 XII, showing accumulation of largely degraded plant litter; arrow points at area containing filamentous cyanobacteria
and G. hueberi (close-up in B). Slide SNSB-BSPG 2016 XII 22. B, Detail of A; tangle of cyanobacteria and G. hueberi (arrow). C, Close-up of
filamentous cyanobacteria often associated with G. hueberi in chert block 2016 XII. Slide SNSB-BSPG 2016 XII 20. D, Largest cluster of G. hueberi
specimens; arrows indicate specimens lacking recognizable bodies but instead containing amorphous black matter. Slide SNSB-BSPG 2015 XVII 3.
E–G, Small clusters of specimens; arrow in E indicates irregularly wrinkled boundary line of vesicle, and arrow in G points at degraded specimen
occurring in the form of a hollow space partially filled with black matter. Slides SNSB-BSPG 2016 XII 12 (E), 2016 XII 35 (F), and 2016 XII 16
(G). H, Informal denotations used for component parts of G. hueberi: v p vesicle, b p bodies, e p envelope. Slide SNSB-BSPG 2008 XVI 43. Scale
bars p 1 cm (A), 200 mm (B), 50 mm (C, E–G), 100 mm (D), 20 mm (H).

delicate dark line (e.g., fig. 2A–C), which is normally smooth but No evidence of structures subtending (giving rise to), ex-
may sometimes also appear to consist of granules (arrow in fig. 2G). tending from, or reaching into the envelope or vesicle from the
Many bodies are surrounded by a whitish halo ca. 1–1.5 mm ambience has been found. One empty specimen shows what
thick (arrows in fig. 2H2, 2H3), which could represent a gelat- appears to be a large opening with a folded-back rim (arrow
inous envelope that formed around the bodies but could also be in fig. 2Q).
an artifact of preservation or microscopy. No evidence has been
found of organic connections between the individual bodies in a
Taxonomy
vesicle. One of the bodies occurs in what appears to be a saclike
envelope (arrows in fig. 2L). While some of the bodies are empty
(fig. 2H, 2O), most have structured contents. However, there is a Glaphyrobalantium M. Krings, gen. nov.
variety in regard to the appearance (and nature?) of the contents, Diagnosis. Spheroidal, ovoid, pyriform, somewhat elongated
both between and within vesicles (e.g., fig. 1H). Some bodies con- (cylindrical), or asymmetrical microfossils comprised of a vesicle
tain a single spot (fig. 2D), an irregular lump, or an amorphous, less than 60 mm long that is bounded by a prominent envelope
often ramifying mass of black or dark brown matter (fig. 2M, (a sheath or massive wall) and typically contains spherical bodies.
2P), while others are characterized by a spot or irregular mass Type species. Glaphyrobalantium hueberi M. Krings (this
of black or dark brown matter surrounded or accompanied by article).
lighter brownish matter (arrows in fig. 2A, 2C, 2F), with the latter
not normally sharply delimited (fig. 2A, 2F). In still other bodies,
Glaphyrobalantium hueberi M. Krings, sp. nov.
only a poorly demarcated (diffluent) area of brownish matter is
present (fig. 2I; arrow in fig. 2N2). Finally, some of the bodies con- Diagnosis. Specimens up to 40 mm in diameter, or up to 55 mm
tain a single spherical structure (4.5–5 mm in diameter) that is long and 35(–40) mm high (in section view); envelope unstrat-
characterized by a darker margin ca. 0.5 mm thick (arrows in ified, less than 1 to 5 mm thick, variable in thickness both within
fig. 2E, 2J, 2K). and between individuals, bounded on outside by delicate, dark
 KRINGS—A CRYPTIC RHYNIE CHERT MICROBIAL FOSSIL 435

line, sometimes additionally covered by diffluent, colorless muci- phied) parental cell undergoes a sequence of repeated divisions
lage; vesicle containing 2–8 (more in large specimens) spherical without intervening growth (Butterfield 2011; Tikhonenkov
or spheroidal bodies; bodies less than 10 mm in diameter, often et al. 2020). If the cells in G. hueberi formed through palintomic
surrounded by whitish halo; bodies empty or with structured cleavage, then the number of cells present in a vesicle reflects
contents; contents variable, ranging from amorphous mass of the number of rounds of division. Moreover, the cells in speci-
dark matter to single spherical structure (4.5–5 mm in diameter) mens containing two or four cells should be distinctly larger
with a darker margin; specimens occur singly or in groups. than the ones in comparably sized specimens containing eight
Holotype. Specimen shown in figure 2A; in slide SNSB- or 16 (or more) cells, but they are not. As a result, there is cur-
BSPG 2016 XII 35, SNSB-Bayerische Staatssammlung für Paläon- rently no evidence to demonstrate either of the three ways to
tologie und Geologie, Munich, Germany. A black arrow on the achieve simple multicellularity in G. hueberi. Another series of
slide indicates the exact position of the specimen. considerations on the nature and affinities of G. hueberi can
Collection locality. Rhynie, Aberdeenshire, Scotland, Na- be offered based on comparison of the basic organization of
tional Grid Reference NJ 494276 (lat. 57720009.9700N, long. the fossil with that seen in other fossil and modern organisms,
002750031.8300W). including encysting protists, fungi and fungus-like organisms,
Stratigraphic position. Dryden Flags Formation. cyanobacteria, and microscopic algae.
Age. Early Devonian; Pragian or earliest Emsian (see Well-
man 2006, 2017; Wellman et al. 2006), 411:5 5 1:3 Ma (Parry
et al. 2011), 407:1 5 2:2 Ma (Mark et al. 2011). Encysting Protists
Etymology. The genus name Glaphyrobalantium (n.), a com-
A certain degree of structural resemblance appears to exist be-
bination of the Greek glaφurός (glaphyrós p elegant, subtle) and
tween G. hueberi and microfossils from the Ediacaran Dou-
balάntion (balántion p money bag, purse), is given because the
shantuo Formation in China described as Tianzhushania and
specimens are reminiscent of small bags filled with coins or
initially interpreted as animal embryos (e.g., Yin et al. 2004).
marbles; the epithet hueberi honors the late Francis (Fran) M.
Developmental evidence from these fossils indicates that hyper-
Hueber (1929–2019) and his preeminent contributions to our
trophied parental cells encysted within a multilayered envelope
understanding of early terrestrial organisms and ecosystems.
and, directly or after a resting period, began a process of coordi-
nated mitotic palintomic cleavage (Huldtgren et al. 2011, fig. 4).
Discussion
Early stages in this process (e.g., the eight-cell stage shown by
these authors in their fig. 2) are slightly reminiscent of G. hueberi,
Various types of microscopic (i.e., less than 100 mm in diame-
albeit the interior cells in the latter fossil are more loosely spaced.
ter) vesicles containing spherical bodies are regularly encountered
Cells resulting from the cleavage process in Tianzhushania even-
in the Rhynie chert, both in the chert matrix and within (de-
tually escaped as propagules, probably through dissolution of the
grading) land plant parts (fig. 3). Making sense of these structures
envelope. Huldtgren et al. (2011) conclude that these fossils are
is generally difficult because they hardly ever reveal how they have
neither animals nor embryos but rather belong outside crown
formed and what would have become of them if they had lived on
group Metazoa, within total group Holozoa (the sister clade to
and not silicified; none of the specimens is physically connected to
Fungi that includes Metazoa, Choanoflagellata, and Mesomy-
structures that can be specifically attributed. Glaphyrobalantium
cetozoea) or perhaps on even more distant branches in the eukary-
hueberi differs from all these fossils primarily in its prominent en-
ote tree. Somewhat similar cysts containing up to 16 cells formed
velope. Unfortunately, the nature of this envelope—whether it is a
through palintomic cleavage have been described in the present-
gelatinous sheath, a wall, or some other type of encasement—
day freshwater opisthokont Syssomonas multiformis (Tikho-
remains obscure.
nenkov et al. 2020, fig. 2m).
The spherical bodies in G. hueberi are most certainly cells of
some kind based on size and shape, which makes the fossil either
a colony or a multicellular phase within a life cycle. Assessing
Fungi and Fungus-Like Organisms
how G. hueberi might have become multicellular, therefore,
could help to narrow the possible affinities by excluding those It is undeniable that the specimens of G. hueberi are slightly
groups of organisms that achieve multicellularity in a different remniscent of asci containing ascospores (Ascomycota). How-
manner. The dynamics of simple multicellularity are usually ever, no evidence has been found to suggest that the structure
characterized as occurring through one of three ways, namely, had yeast growth, that it was borne on a hypha or filament, or
by aggregation, through the formation of a coenocyte and sub- that it developed in some type of fungal fruiting body, such as
sequent cellularization, or by palintomy (Xiao 2002; Chen et al. a cleistothecium. Neither is there any evidence that G. hueberi
2014; Ostrowski 2020). Glaphyrobalantium hueberi does not represents some type of fungal reproductive unit in itself, for in-
appear to have formed through aggregation because there is stance, a sporocarp containing spores.
no evidence of cellular clusters that are not surrounded by an en- The bodies in G. hueberi are similar in overall appearance
velope. Moreover, swarmers, initially at least, would not neces- and content variability to the bodies occurring in three other,
sarily form such distinctive enclosures as seen in the fossils. A albeit distinctly larger, microfossils from the Rhynie chert, namely,
coenocyte develops from a parental cell that undergoes multiple Nimbosphaera rothwellii, a putative chytrid zoosporangium con-
nuclear divisions prior to cellularization (e.g., Ondracka et al. taining zoospores (Harper and Krings 2019), and Frankbaronia
2018), so one might expect to see at least some G. hueberi spec- polyspora and Frankbaronia velata, two oomycotan oogonia
imens preserved prior to completion of the cellularization phase. containing oospores (Krings et al. 2012, 2013). Nimbosphaera
Finally, palintomy is a process during which a large (hypertro- rothwellii is described as a vesicle containing spheroidal bodies
 Fig. 2 Morphology of Glaphyrobalantium hueberi from the Lower Devonian Rhynie chert. A, Holotype specimen; arrows indicate bodies con-
taining black or dark brown matter surrounded or accompanied by lighter brown matter. Slide SNSB-BSPG 2016 XII 35. B, C, Specimens exhibiting
varying body contents; arrow in C indicates dark brown matter surrounded by lighter brownish matter. Slide SNSB-BSPG 2016 XII 6. D, Specimen
showing irregular envelope, in places covered by what appears to be diffluent, colorless mucilage (arrow). Slide SNSB-BSPG 2016 XII 16. E, J, K, Bodies
containing single spherical structure with a dark margin (arrows). Slides SNSB-BSPG 2016 XII 22 (E), 2008 XVI 48 (J), and 2008 XVI 43 (K). F, Body
containing irregular mass of black matter accompanied by lighter brownish matter (arrow). Slide SNSB-BSPG 2016 XII 35. G, Body bounded by line
apparently consisting of granules (arrow). Slide SNSB-BSPG 2016 XII 35. H1–3, Specimen containing eight bodies (labeled 1–8) in three different focal
planes; arrows in H2 and H3 indicate whitish halo around bodies. Slide SNSB-BSPG 2016 XII 35. I, Specimen lacking most of envelope. Slide SNSB-
BSPG 2016 XII 6. L, Specimen with body enclosed in saclike envelope (arrows). Slide SNSB-BSPG 2008 XVI 43. M, Bodies containing spot, irregular
lump, or ramified mass of black matter. Slide SNSB-BSPG 2016 XII 35. N1–3, Detail of figure 1F; middle specimen in three different focal planes, showing
 KRINGS—A CRYPTIC RHYNIE CHERT MICROBIAL FOSSIL 437

(zoospores) and enveloped in a wide sheath and hence is rather

similar to G. hueberi also in regard to basic organization. How-
ever, extending from some of the specimens are bulbous append-
ages and rhizoids, both of which have not been observed in
G. hueberi. While there is no envelope or sheath in F. polyspora
(Krings et al. 2012), the oogonia of F. velata are covered in thick,
consolidated mucilage (Krings et al. 2013). However, F. velata
differs from G. hueberi in that it possesses a truncated extension
(neck region), which represents the attachment site of the paren-
tal hypha or stalk. While affinities of G. hueberi to protists, fungi,
and fungus-like organisms cannot be ruled out, it seems much
more likely to me, based on morphology and habitat, that this
fossil represents a colony with affinities to either the cyanobac-
teria or eukaryotic microalgae and that the bodies inside the ves-
icle are cyanobacterial or algal cells, respectively.

Fig. 3 Different types of microscopic vesicles containing spherical

Cyanobacteria bodies from the Rhynie chert. Slides SNSB-BSPG 2016 XII 35 (A–C),
2016 XII 21 (D), BayRy 3 (E), and 2013 V 156 (F). Scale bars p 10 mm.
One structural feature that has been used to distinguish be-
tween fossil cyanobacteria and eukaryotic microalgae results
from the fact that cyanobacterial cells, unlike algal cells, cave like” (Geitler 1932, p. 206). Fossil morphological equivalents
in upon death and shrink to a small polyhedral or star-shaped to such Gloeocapsa colonies have been described as Clono-
body, because cyanobacterial cell walls are composed of repeat- phycus (Oehler 1977, fig. 11A–11D, 11J–11K, 1978, fig. 5A–
ing peptidoglycan units that are directly exposed to osmotic 5C) and Eogloeocapsa (Sergeev 1994; Sergeev et al. 2012, pl. 5,
pressure (Golubic and Barghoorn 1977; Knoll and Golubic 1–4; Knoll et al. 2013, fig. 6C) and date back to at least the
1992). Fossil cyanobacteria, therefore, typically occur in the Mesoproterozoic. Another Precambrian cyanobacterial fossil
form of EPS (pextracellular polymeric substance) envelopes that may occur in small colonies similar to G. hueberi is Gloeo-
and sheaths, which are not part of the osmotic system of the cells diniopsis lamellosa, which has been compared with present-day
and hence collapse more evenly and faithfully preserve the Chroococcus, Gloeocapsa, and Entophysalis (Sergeev et al.
shapes of cells and colonies (Sergeev et al. 2012; Krings and 2012, pls. 7, 6, text fig. 21; Cui et al. 2020, figs. 4, 5a, 5b).
Harper 2019). The envelopes/sheaths may contain remnants The lack of evidence of cell division in the form of transverse
of the actual cells in the form of small inclusions. The structured binary fission (e.g., equatorial constriction, cross-wall forma-
contents of the G. hueberi bodies are rarely similar to, and much tion, and cell separation; see Golubic et al. 1995, fig. 2; Cepák
more variable in appearance than, the inclusions seen in bona and Komárek 2010, figs. 1–5) argues against the interpretation
fide cyanobacteria from the Rhynie chert (e.g., fig. 1C; Croft of G. hueberi as a cyanobacterium. Moreover, EPS envelopes
and George 1959, pls. 42–44; Krings et al. 2007, pl. I, 3–7; that are persistent through several cell divisions and give rise
Taylor and Krings 2015, text fig. 2; Krings and Harper 2019, to cell groups preserving a record of their division history, as
fig. 3a–3f; Krings 2021c, pl. I, 5–7). One the other hand, there seen in Gloeocapsa, are not recognizable in G. hueberi. It is pos-
exists a high level of morphological congruence between G. hue- sible, however, that G. hueberi represents a status solutus, as
beri and certain present-day chroococcalean cyanobacteria, in- recorded for G. alpina by Brand (1900), in which the individual
cluding species of Asterocapsa, Aphanothece, Gloeocapsa, and envelopes all dissolve so that the cells are embedded in a com-
Gloeothece that occur in the form of multicellular groups or col- mon, uniform gelatinous mass.
onies of cells surrounded by a colonial envelope or sheath (Ko-
márek and Anagnostidis 1998; Komárek and Johansen 2015;
Microscopic Algae
Kumar et al. 2018, fig. 1a–1f ). Particularly well-suited equiv-
alents seem to me to be certain species of Gloeocapsa, such as Colonial sheaths enveloping small groups or colonies of cells
Gloeocapsa alpina (Wygasch 1958, fig. 14) and Gloeocapsa are also known to occur in certain freshwater and aerial unicel-
sanguinea (Oeggl 1986, fig. 18; Popović et al. 2017, fig. 3d), lular algae, including several present-day species of the genus
which form microscopic colonies (up to 40 mm in diameter) of Gloeocystis (Chlorophyta; Sphaeropleales) that are similar mor-
two to eight (sometimes more) cells. Cells and their immediate phologically to the fossil. These algae form spheroidal colo-
groups are surrounded by EPS envelopes, which are usually la- nies comprised of two to eight (rarely more) cells enveloped in
mellate, and the colonies are enveloped in a wide colonial sheath colorless mucilage and often bounded by a distinct mucilaginous
(Golubić 1965; Whitton 2011; Komárek and Johansen 2015), colonial sheath (Comère 1912, pl. XII, 3a, 3b; Hindák 1978,
the outer boundary layer of which has been denoted “cuticle- figs. 1, 2.1; Kim 2014, fig. 6a, 6b, 6f ). However, maybe the

poorly demarcated (diffluent) area of brownish matter in several bodies (arrow in N2) and papilla-like protrusion of envelope (in N1). Slide SNSB-BSPG
2016 XII 35. O1–5, Pyriform specimen containing mostly empty bodies in five different focal planes; note surface view (O5), suggestive of surface or-
namentation composed of fine reticulations. Slide SNSB-BSPG 2016 XII 22. P, Specimen containing more than 30 bodies. Slide SNSB-BSPG 2016 XII
35. Q, Detail of figure 1D; empty specimen showing what appears to be a large opening with folded-back rim (arrow). Slide SNSB-BSPG 2015 XVII 3.
Scale bars p 10 mm.
438 INTERNATIONAL JOURNAL OF PLANT SCIENCES

envelope in G. hueberi is not a sheath but rather a massive cell Irrespective of the systematic affinities, the high recognition
wall. For example, the nonmotile vegetative cells in the green al- value of G. hueberi provokes the question as to whether this fossil
gal genus Chlorococcum (Chlorophyta; Chlamydomonadales) could possibly also be obtained through palynological sampling.
are known to have thin walls when young, but as they attain Dispersed palynomorphs (including phytodebris), recovered by
their full size and grow older, the walls sometimes become acid maceration of sediment, are well known from the Rhynie se-
successively thicker and stratified (Archibald and Bold 1970, quence (Wellman 2006, 2017; Wellman et al. 2019; Wellman and
figs. 39, 47, 93; Santhoshkumar et al. 2016, fig. 1A; Maltsev Ball 2021). However, fossils comparable to G. hueberi have, to
and Konovalenko 2017, fig. 1C). Arguing against the interpreta- my knowledge, not been described. There are several possible ex-
tion of the G. hueberi envelope as a cell wall is perhaps that its planations for this. Perhaps G. hueberi occurred in areas of the
thickness often varies considerably within one individual (e.g., Rhynie ecosystem that are not reflected by the sediment samples
fig. 2A, 2D), but these variations could just as well be a postmor- used hitherto for palynological sampling. It is also possible that
tem artifact resulting from shrinkage of the vesicle and desicca- G. hueberi was fragile (e.g., if it were a cyanobacterial or algal col-
tion of the envelope. ony held together by a gelatinous sheath) and readily destroyed to
The life cycle of G. hueberi remains largely obscure because unrecognizable condition by mechanical forces during fossiliza-
all specimens appear to be in approximately the same stage of tion or chemically during maceration or that it was short lived
development. However, one feature that shows some level of (e.g., if it were a transitory phase in a life cycle) and thus generally
variability among the specimens is the number of bodies in the unlikely to become preserved.
vesicle, which ranges from two to more than 30. If the interpre-
tation of G. hueberi as a cyanobacterium or eukaryotic alga is Conclusions
accurate, then it is probable that this variability reflects a devel-
opmental sequence, namely, that the number of bodies (cells) in- Resolving the systematic affinity of a fossil microorganism and
creased through successive cell divisions within the vesicle, begin- understanding its biology and ecology—if at all possible—may
ning with a single-celled stage. This latter stage, however, has not take a long time because microbial fossils are rarely preserved
yet been identified in the Rhynie chert, likely because it does not either in sufficient numbers or in a way that provides insights into
show the whole set of structural features by which G. hueberi is all phases of growth and reproduction. Glaphyrobalantium hue-
characterized. If the interpretation of the specimen shown in fig- beri exemplifies this dilemma. The fossil is generally well pre-
ure 2Q is correct, then it is furthermore reasonable to assume served, and there are more than 150 specimens available to
that the bodies (cells) were liberated from the parental vesicle study. This notwithstanding, the affinity and life history of the
at some point, perhaps as a result of the increasing pressure organism remain conjectural. All specimens exhibit approxi-
and tightness of space in the vesicle. A similar developmental se- mately the same basic morphology, and there are hardly any in-
quence has been documented for the Cambrian acanthomorphic dividuals or traits as yet recognized that enable conclusions to be
acritarch Yurtusia uniformis from China (Dong et al. 2009, fig. 5.5– drawn on other stages of the life cycle. In spite of these limita-
5.16). Shang et al. (2020) have recently used size differences tions, it is worthwhile to describe microfossils like G. hueberi be-
and morphology, along with single or multiple bodies present cause they can be used to measure past biodiversity based on
in several of their specimens, to suggest that Y. uniformis was a morphological distinctiveness. Morphology represents the sole
unicellular green alga (Chlorophyta) that reproduced asexually comprehensive proxy indicator of past microbial biodiversity
through the production of autospores, that is, nonmotile spores and thus is critical to subsequent studies assessing the roles that
that form through the internal division of a single cell (the auto- microorganisms have had as constituents of ancient ecosystems. I
sporangium) and possess the same shape as the parental cell be- anticipate that some of the complex processes and interdepen-
fore liberation (Ettl 1988; Tschermak-Woess 1989). Specimens dencies that governed the Rhynie paleoecosystem during the Early
containing more than two bodies (autospores) formed either Devonian will be understood more fully as more microbial morphol-
through cell division by multiple fission after two or more nuclear ogies are described and documented and will provide increasing
divisions or by autospore propagation inside the mother cell, opportunities to relate fossils to extant equivalents and ultimately
which resulted in compound colonies comprised of cells of different help to formulate or refine ideas about the biology and ecology of
developmental stages. Several other types of acritarchs containing the fossil forms. This is the same philosophy that was so much a part
bodies have also been interpreted as algal sporangia (including of the scientific work of Fran Hueber, to whom I dedicate this arti-
autosporangia) with possible affinities to the Chlorophyta (e.g., cle. His skill in acquiring and documenting information on ancient
Kaźmierczak and Kremer 2009; Kremer et al. 2012; Moczy- organisms, and providing detailed descriptions and critical evalu-
dłowska and Liu 2021). While it is conceivable, therefore, that ations, will always have my deep admiration.
G. hueberi was a unicellular eukaryotic alga and produced auto-
spores in thick-walled mother cells (autosporangia), no evidence Acknowledgments
of successive generations of autosporangia occurring inside one
another has been found in the specimens containing more than I thank H. Martin and S. Sónyi (both Munich, Germany) for
two bodies, except possibly for the saclike envelope enclosing technical assistance. Insightful comments by P. Strother (Weston,
one of the bodies in the specimen shown in figure 2L. MA) and an anonymous reviewer are greatly appreciated.

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