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Acritarch Evidence for an Ediacaran Adaptive Radiation of Fungi

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Acritarch Evidence for an Ediacaran Adaptive Radiation of Fungi Botanica Pacifica. A journal of plant science and conservation. 2015. 4(2): 19–33 DOI: 10.17581/bp.2015.04203 Acritarch Evidence for an Ediacaran Adaptive Radiation of Fungi Gregory J. Retallack Gregory J. Retallack ABSTRACT e-mail: [email protected] Acritarchs are problematic organic-walled microfossils, traditionally regarded as phytoplankton, but also as cysts of metazoans or mesomycetozoans, and fungi. Department of Geological Sciences, This review develops criteria for distinguishing these alternatives, and documents University of Oregon, Eugene, Oregon fungal features in several Precambrian acritarchs: (1) irregular shape, (2) hyphal 97403-1272, U.S.A. attach ment, (3) spherical wall protrusions, (4) septate and fused hyphae, (5) multilayered brittle walls that split and detach, (6) large size (>100 μm), and (7) chitin and chitosan composition revealed by FTIR. Large acritarchs with fungal features are common and diverse during the Ediacaran, at the same time as extinct lichenlike Vendobionta. A different assemblage of small acritarchs di- ver sified with the Cambrian evolutionary explosion of algae and metazoans. A Manuscript received: 16.07.2015 Review completed: 14.08.2015 fos sil record of glomeromycotan fungi back to the Paleoproterozoic (2200 Ma) Accepted for publication: 17.08.2015 supports the idea of fungal life on land long before land plants, and an amended Published online: 20.08.2015 version of Pirozynski and Malloch’s mycotrophic origin of early land plants. Keywords: acritarch, Ediacaran, Glomeromycota, FTIR, wall ultrastructure РЕЗЮМЕ Реталлак Г.Дж. Акритархи подтверждают адаптивную радиацию грибов. Акритархи – проблемные микрофоссилии c ор га ническими кле­ точ ными стенками, традиционно рассматриваются как фи топланктон, а так же как цисты многоклеточных организмов, мезомице то в и грибов. Дан- ный обзор предлагает критерии для различения этих групп организмов и анализ признаков нескольких групп докембрийских акритарх: (1) непра- вильная форма, (2) крепление гиф (3) сферические выступы клеточных стенок, (4) цельные гифы и гифы с перегородками (5) многослойные хруп- кие и расслаивающиеся покровы (6) большой размер (> 100 мкм) и (7) со- держание хитина и хитозана, выявляемое инфракрасной спектроксопией. Большие акритархи с признаками грибов обычны и разнообразны в эдиа- карской биоте, в то время как лихеноподобные организмы малочисленны. Сооб щества небольших акритарх достигли наибольшего разнообразия во время кембрийского эволюционного взрыва водорослей и многоклеточ- ных. Находки окаменелостей гломеромицетов вплоть до палеопротерозоя (2200 млн лет) поддерживают идею распространения жизни на суше в виде грибов задолго до наземных растений и говорят в пользу версии происхож- дения ранних наземных растений от микотрофных организмов, согласно Пирозинскому и Маллоку. Ключевые слова: акритархи, эдиакарский период, гломеромицеты, инфра- красная спектроскопия, ультраструктура клеточных стенок Переведено редколлегией INTRODUCTION not preserve microscopic reproductive structures of fungi, so a more promising source of biological information is the Molecular clocks now place the antiquity of fungi at suggestion of Pirozynski (1976), Hermann (1979), Locquin about 2500–1000 Ma (Taylor & Berbee 2006, Blair 2009, (1983), Burzin (1993) and Butterfield (2005) that there is a Berbee & Taylor 2010). Other evidence for Proterozoic Precambrian record of fungi among the enigmatic mic ro- fungi have come from fossil compressions such as 2200 Ma fos sil palynomorphs known as acritarchs (Grey 2005, Moc- Dis kagma (Retallack et al. 2013a), and 1480 Ma Horodyskia zyd łowska et al. 2011). This study follows the approach of (Retallack et al. 2013b), permineralizations such as 2600– Butterfield (2005) in reviewing benchmarks in the fossil 575 Ma Eomycetopsis (Mendelson & Schopf 1991, Alter­ re cord for particular fungal and animal-fungal characters, mann & Schopf 1995), and Vendobionta such as 565 Ma inclu ding hyphal attachment and fusion, bulbous wall pro- Frac ti fusus (Peterson et al. 2003, Gehling & Narbonne 2007) tru sions, and brittle fracture. Also included is discovery of and 550 Ma Dickinsonia (Retallack 2007, 2013a). All these mul tilayered wall ultrastructure viewed by TEM and chitin records are taxonomically unsatisfactory because they do com position revealed by FTIR (Table 1). This study also ©Botanical Garden-Institute FEB RAS. 2015. Special issue “Plant evolution at levels from molecular to ecosystem” 19 Retallack Table 1. Sources of FTIR spectra Species Higher taxon Age Reference Multifronsphaeridium pelorum “acritarch” Ediacaran Arouri et al. 1999 Leiosphaeridium jacutica “acritarch” Ediacaran Marshall et al. 2005 Satka squamulifera “acritarch” Ediacaran Marshall et al. 2005 Shuiyousphaeridium macroreticulatum “acritarch” Ediacaran Marshall et al. 2005 Botryococcus braunii “acritarch” Permian Lin & Ritz 1993 Tasmanites punctatus “acritarch” Permian Lin & Ritz 1993 Mucor rouxii Mucorales, Zygomycota modern Wu et al. 2005 Rhizopus stolonifer Mucorales, Zygomycota modern Kaminskyj et al. 2008 Fusarium avenaceum Hypocreales, Ascomycota modern Calderón et al. 2009 Metapenaeopsis dobsoni Decapoda, Arthropoda modern Sini et al. 2007 Bombus terrestris Hymenoptera, Arthropoda modern Matján et al. 2007 Protoceratium reticulatum Gonyaulacales, Dinoflagellata modern Domenighini & Giordano 2009 Symbiodinium microadriaticum Suessiales, Dinoflagellata modern Domenighini & Giordano 2009 Chlamydomonas reinhardtii Volvocales, Chlorophyta modern Domenighini & Giordano 2009 Chlorella marina Chlorellales, Chlorophyta modern Domenighini & Giordano 2009 tabulates the changing diversity of acritarchs and other un usual element of ornament. These elongate elements plausible fun gal megafossils as a proxy for evolutionary are hollow and open into the interior of the vesicle (Fig. radiations in Pre camb rian fungi. 1 E,1: G H), so they are not surficial elaborations of the Acritarchs, like many palynomorphs, are an acknow led- wall. Nor do they appear to be tubular structures spearing ged taxonomic wastebasket for spheroidal organic-walled the vesicle, as suggested by Cavalier­Smith (2006), because microfossils of unknown affinities (Grey 2005). Sug gested they flare into the outer walls. The form­generic name Ger­ affinities of acritarchs include Dinoflagellata, Pra si no phy­ mi no sphaera (Fig. 1 H) implies that the tubular feature was a ceae, Chlorophyceae, Fungi, Mesomycetozoa, and Me ta zoa. ger mi nation tube, but that is an unlikely explanation given Dinoflagellates, prasinophytes and chlorophytes are aqua­ the comparable thickness and cutinization of walls of both tic eukaryotic phytoplankton (Moczydłowska et al. 2011). the narrow tube and the large spherical body of the vesicle. Fungi are marine and terrestrial, eukaroytic de com po sers, These long filaments of comparable materials to the and include acritarch-like structures in Glo me ro myco ta, sphe ri cal vesicle are similar to hyphae of Glomeromycotan orders Glomales (mycorrhizae: Wu et al. 1995), and Ar- spores, saccules and vesicles (Wu et al. 1995, Walker et al., chaeo sporales (Geosiphon: Schüßler 2012), and Muco ro my- 2004, Sieverding & Oehl 2006, Pereyra et al. 2006, Schüßler co tina (classification of Hibbett et al. 2007), Order Mu co ra­ 2012). Similar basal tubular strucutres and wall extensions les (molds: Pereyra et al. 2006). Mesomycetozoa are most ly are also found in the 2200 Ma problematicum Diskagma fish parasites, but include spores with palintomic clusters (Reta llack et al. 2013 a). Neither algae, mesomycetozoans, of cells deceptively similar to animal embryos (Huldtgren nor metazoans emerging from encystment construct single et al. 2011). Choanoflagellates and arthropods, pro duce thick­walled tubes markedly narrower than the cyst (Cohen acritarch-like diapause cysts around embryos with cell dif- et al. 2009, Huldtgren et al. 2011). feren tiation (Cohen et al. 2009). This review suggests that Hyphal fusion some acritarchs were fungi, but other acritarchs were pro- bab­­ly algae, mesomycetozoans and metazoans. As for pa ly- Sparsely septate hyphae which loop and fuse beyond no logical identifications, distinctive criteria are needed, and the vesicle wall are best documented in palynomorphs of several are suggested here. Tappania sp. (Butterfield 2005), which has the geologically oldest known examples of this feature (at 820 ± 10 Ma). DIAGNOSTIC FUNGAL FEATURES These hyphae form a three dimensional net around the The following features are considered diagnostic of fun­­ vesicle from amalgamation of hyphae diverging at high gi, as opposed to algae, Mesomycetozoa or Metazoa, and may angles to loop back toward the vesicle: open loops and constrain their geological antiquity in the fossil re cord. unfused branches have been interpreted as an unfinished process of hyphal fusion and elaboration (Butterfield 2005). Hyphal attachment Hyphal fusion of sparsely septate hyphae is not evidence A distinctive feature of fungal chlamydospores are of higher fungi (Dikarya = Ascomycota + Basidiomycota), attached tubular structures (hyphae) much longer than sur- as once thought by Butterfield (2005), because it has also ficial spines or other ornament (Fig. 1: A–D). Tappania plana been reported in Glomeromycota (Bever & Wang 2005). (Ja vaux et al. 2001) has the geologically oldest example of Hyphal fusion is also found in Oomycota, which are no such features (at 1466 ± 18 Ma). Such features are also longer regarded as Fungi, but as Heterokonta (Cavalier­ characteristic
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