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Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event.

ABSTRACT: Large, architecturally complex lichen symbioses arose only a few times in evolution, increasing thallus size by orders of magnitude over those from which they evolved. The innovations that enabled symbiotic assemblages to acquire and maintain large sizes are unknown. We mapped morphometric data against an eight-locus fungal phylogeny across one of the best-sampled thallus size transition events, the origins of the Placopsis lichen symbiosis, and used a phylogenetic comparative framework to explore the role of nitrogen-fixing cyanobacteria in size differences. Thallus thickness increased by >150% and fruiting body core volume increased ninefold on average after acquisition of cyanobacteria. Volume of cyanobacteria-containing structures (cephalodia), once acquired, correlates with thallus thickness in both phylogenetic generalized least squares and phylogenetic generalized linear mixed-effects analyses. Our results suggest that the availability of nitrogen is an important factor in the formation of large thalli. Cyanobacterial symbiosis appears to have enabled lichens to overcome size constraints in oligotrophic environments such as acidic, rain-washed rock surfaces. In the case of the Placopsis fungal symbiont, this has led to an adaptive radiation of more than 60 recognized species from related crustose members of the genus Trapelia. Our data suggest that precyanobacterial symbiotic lineages were constrained to forming a narrow range of phenotypes, so-called cryptic species, leading systematists until now to recognize only six of the 13 species clusters we identified in Trapelia.

SUBMITTER: Schneider K

PROVIDER: S-EPMC5324663 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event.

Schneider Kevin K Resl Philipp P Spribille Toby T

Molecular ecology 20160511 14

Large, architecturally complex lichen symbioses arose only a few times in evolution, increasing thallus size by orders of magnitude over those from which they evolved. The innovations that enabled symbiotic assemblages to acquire and maintain large sizes are unknown. We mapped morphometric data against an eight-locus fungal phylogeny across one of the best-sampled thallus size transition events, the origins of the Placopsis lichen symbiosis, and used a phylogenetic comparative framework to explo ...[more]

PMID: 27037681

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Project description:UNLABELLED:The "Candidatus Synechococcus spongiarum" group includes different clades of cyanobacteria with high 16S rRNA sequence identity (~99%) and is the most abundant and widespread cyanobacterial symbiont of marine sponges. The first draft genome of a "Ca. Synechococcus spongiarum" group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, "Ca. Synechococcus spongiarum" includes a variety of clades that may differ widely in genomic repertoire and consequently in physiology and symbiotic function. Here, we present three additional draft genomes of "Ca. Synechococcus spongiarum," each from a different clade. By comparing all four symbiont genomes to those of free-living cyanobacteria, we revealed general adaptations to life inside sponges and specific adaptations of each phylotype. Symbiont genomes shared about half of their total number of coding genes. Common traits of "Ca. Synechococcus spongiarum" members were a high abundance of DNA modification and recombination genes and a reduction in genes involved in inorganic ion transport and metabolism, cell wall biogenesis, and signal transduction mechanisms. Moreover, these symbionts were characterized by a reduced number of antioxidant enzymes and low-weight peptides of photosystem II compared to their free-living relatives. Variability within the "Ca. Synechococcus spongiarum" group was mostly related to immune system features, potential for siderophore-mediated iron transport, and dependency on methionine from external sources. The common absence of genes involved in synthesis of residues, typical of the O antigen of free-living Synechococcus species, suggests a novel mechanism utilized by these symbionts to avoid sponge predation and phage attack. IMPORTANCE:While the Synechococcus/Prochlorococcus-type cyanobacteria are widely distributed in the world's oceans, a subgroup has established its niche within marine sponge tissues. Recently, the first genome of sponge-associated cyanobacteria, "Candidatus Synechococcus spongiarum," was described. The sequencing of three representatives of different clades within this cyanobacterial group has enabled us to investigate intraspecies diversity, as well as to give a more comprehensive understanding of the common symbiotic features that adapt "Ca. Synechococcus spongiarum" to its life within the sponge host.

Dataset Information

Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event.

Publications

Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event.

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