Coleofasciculaceae, a Monophyletic Home for the Microcoleus steenstrupii Complex and Other Desiccation-tolerant Filamentous Cyanobacteria

Cyanobacteria classified as Microcoleus steenstrupii play a significant role as pioneers of biological soil crusts (biocrusts), but this taxon is recognized to constitute a diverse complex of strains and field populations. With the aim of clarifying its systematics, we conducted a polyphasic characterization of this and allied taxa. A 16S ribosomal gene meta-analysis of published environmental sequences showed that the complex encompasses a variety of well supported genus-level clades with clade-specific environmental preferences, indicating significant niche differentiation. Fifteen strains in the M. steenstrupii complex were selected as representative of naturally occurring clades and studied using 16S rRNA gene phylogeny, morphology, and niche delineation with respect to temperature and rainfall. Bayesian phylogenetic reconstructions within a comprehensive, curated database of long 16S rRNA cyanobacterial sequences (1,000 base pairs or more) showed that they all belonged in a monophyletic, family-level clade (91.4% similarity) that included some other known genera of desiccation-resistant, largely terrestrial, filamentous, nonheterocystous cyanobacteria, including Coleofasciculus, the type genus for the family Coleofasciculaceae. To accommodate this biodiversity, we redescribe the Coleofasciculaceae, now composed of 11 genera, among which six are newly described herein (Funiculus, Parifilum, Arizonema, Crassifilum, Crustifilum, and Allocoleopsis), and five were previously recognized (Porphyrosiphon, Coleofasciculus, Pycnacronema, Potamolinea, and Wilmottia). We provide an evaluation of their respective niches and global distributions within biocrusts based on published molecular data. This new systematics treatment should help simplify and improve our understanding of the biology of terrestrial cyanobacteria.