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First published online July 10, 2009; doi:10.3732/ajb.0800258 American Journal of Botany 96: 1409-1418 (2009) © 2009 Botanical Society of America, Inc.

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Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria¹

² Department of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605-2496 USA ³ Department of Environmental Science and Policy, George Mason University, Fairfax, Virginia 22030-4444 USA ⁴ Laboratorio de Hongos, Instituto Nacional de Biodiversidad (INBio), Apdo. 22-3100, Santo Domingo de Heredia, Costa Rica ⁵ Botanisches Museum Berlin Dahlem, Königin-Luise-Strasse 6-8, D-14191 Berlin, Germany ⁶ Botany Department, Charles Darwin Foundation (AISBL), Puerto Ayora, Santa Cruz, Galápagos, Ecuador

ABSTRACT

Phylogenetic diversity of lichen photobionts is low compared to that of fungal counterparts. Most lichen fungi are thought to be associated with just four photobiont genera, among them the cyanobacteria Nostoc and Scytonema, two of the most important nitrogen fixers in humid ecosystems. Although many Nostoc photobionts have been identified using isolated cultures and sequences, the identity of Scytonema photobionts has never been confirmed by culturing or sequencing. We investigated the phylogenetic placement of presumed Scytonema photobionts and unicellular morphotypes previously assigned to Chroococcus, from tropical Dictyonema, Acantholichen, Coccocarpia, and Stereocaulon lichens. While we confirm that filamentous and unicellular photobiont morphotypes belong to a single clade, this clade does not cluster with Scytonema but represents a novel, previously unrecognized, highly diverse, exclusively lichenized lineage, for which the name Rhizonema is available. The phylogenetic structure observed in this novel lineage suggests absence of coevolution with associated mycobionts at the species or clade level. Instead, highly efficient photobiont strains appear to have evolved through photobiont sharing between unrelated, but ecologically similar, coexisting lineages of lichenized fungi ("lichen guilds"), via the selection of particular photobiont strains through and subsequent horizontal transfer among unrelated mycobionts, a phenomenon not unlike crop domestication.

Key Words: Acantholichen • Coccocarpia • cyanobacteria • Dictyonema • lichens • Nostoc • rDNA sequence analyses • Scytonema • symbiosis • neotropics

Received for publication 24 July 2008. Accepted for publication 31 March 2009.

FOOTNOTES

¹ Material used in this study was collected in Guatemala, Costa Rica, Peru, Bolivia, and The Philippines, in the framework of three NSF grants to The Field Museum: DEB 0206125 (PI R.L.), DEB 0516116 (PI Thorsten Lumbsch, Co-PI R.L.), and DEB 0715660 (PI R.L.), and with support by the OTS for a tropical lichen workshop in Las Cruces, Costa Rica. The Costa Rican MINAE and SINAC, as well as INBio, are thanked for their support and cooperation in obtaining permits for collecting and DNA studies. The Galápagos National Park Service provided specimens permits for analysis. F.B. is particularly grateful to National Park Director E. Muñoz and Technical Director W. Tapia for continued support of the Galápagos lichen inventory. Specimens were collected in the Galápagos Islands with support from a National Geographic Research Grant 8162–07 to F.B. This is a Charles Darwin Research Station publication with CDRS no. 1088. F. Barrie is kindly thanked for nomenclatural advice.

⁷ Author for correspondence (e-mail: rlucking{at}fieldmuseum.org)

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