Geography and climate drive the distribution and diversification of the cosmopolitan cyanobacterium Microcoleus (Oscillatoriales, Cyanobacteria)

ABSTRACT

Despite the extensive diversity of bacteria and their importance to the fundamental functioning of terrestrial ecosystems, their distribution patterns are still not fully known. To fill the gap and further understand the biogeographic patterns in bacteria, we investigated the phylogeographic structure and the underlying drivers of diversification among populations of the cyanobacterium Microcoleus spp. The phylogenetic history was reconstructed using 16S rRNA genes and the 16S–23S internal transcribed spacer (ITS) of 495 Microcoleus spp. isolates. Ancestral area and state reconstruction was employed to investigate the distributional and ecological patterns within Microcoleus. Both isolation by distance and isolation by environment were tested with distance matrices analysis. The phylogenetic signal tests were conducted in order to assess the influence of the climatic preferences on the diversification of Microcoleus isolates. The distribution and phylogenetic diversification of Microcoleus are driven by both isolation by distance and environment, leading to at least 13 distinct lineages that could represent novel cyanobacterial species. Microcoleus spp. exhibited a distinct phylogeographic structure within the respective lineages. The ancestral area and state reconstruction revealed that Microcoleus most likely arose in Europe in terrestrial habitats. The phylogenetic signal showed that the phylogeny significantly affects the climatic preferences of Microcoleus strains. Geographic distance and contemporary climatic conditions play significant roles in shaping the distribution and diversification of Microcoleus. The observed patterns of distribution may shift in the future due to the impact of climate change.

Highlights

• Microcoleus exhibited distinct phylogeographic structure within the respective lineages.

• Geographic and environmental heterogeneity affect Microcoleus distribution and diversification.

• Genetically distinct lineages coexist at the same site.

KEYWORDS:

• Algae
• allopatry
• biogeography
• blue-green algae
• culture
• diversity
• microbial diversity
• microbial ecology
• microbial mats
• Microcoleus vaginatus

Acknowledgements

We would like to thank Kateřina Čapková and Klára Řeháková (Institute of Hydrobiology, Czech Academy of Sciences, Czech Republic) who provided samples from India and USA, Jan Kollár (Palacký University Olomouc, Czech Republic) who provided samples from Norway and Ivo Sedláček, Michal Zeman and Barbora Chattová (Masaryk University Brno, Czech Republic) who provided samples from Antarctica. We would also thank Dale A. Casamatta (University of North Florida, USA) for language correction and comments on the manuscript and samples from the USA.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary information

The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2021.2007420

Supplementary table S1: List of the Microcoleus spp. strains, GPS locations, habitats, accession numbers of 16S and 16S-23S ITS sequences.

Supplementary table S2: Extracted values of bioclimatic variables (downloaded from WorldClimv2.1) in R with the package ‘raster’ for Microcoleus spp. strains in this study.

Supplementary table S3: A number of strains in each of Microcoleus spp. lineages identified in this study

Supplementary table S4: A number of lineages found in environmental samples of Microcoleus spp. and the list of countries or regions where samples were collected.

Supplementary table S5: Summary of the phylogenetic signal measurement analysis for 19 bioclimatic variables (with Pagel’s λ, Abouheif’s C_mean, and Moran’s I) used to detect the presence of the phylogenetic signal in the climatic nice space of Microcoleus spp. Highlighted bioclimatic variables were not auto-correlated.

Supplementary fig. S1. Phylogenetic tree inferred from the maximum-likelihood (ML) analysis based on 16S rRNA and 16S-23S ITS sequences. Asterisks at the nodes indicate maximum likelihood bootstrap support (≥ 0.99). Based on the monophyletic criterion, strains were associated with thirteen lineages (1-13). The outgroup is indicated as O. Strains forming singleton nodes are indicated as #. Scale bar indicates substitutions per site.

Supplementary fig. S2. Summary of the ancestral area reconstruction analysis based on Bayesian Binary MCMC (BBM) model in Microcoleus spp. The ancestral areas with the highest likelihood are represented within node pies. Colour code corresponds to the following regions: (A) Europe, (B) North America, (C) Africa, (D) Asia, (E) Arctic, (F) Antarctic, (G) Australia. The black asterisk represents other ancestral areas. Additional colours within the colour code correspond to the multiple region areas (AD).

Supplementary fig. S3. Summary of the ancestral character state reconstruction analysis based on Bayesian Binary MCMC (BBM) model in Microcoleus spp. The ancestral habitats with the highest likelihood are represented within node pies. Colour code corresponds to the following habitats: (A) puddle, (B) soil, (C) concrete, (D) moss vegetation, (E) rocks. The black asterisk represents other ancestral habitats. Additional colours within the colour code correspond to the multiple character states (AB, AE, BC).

Author contributions

A. Stanojković: culture isolation and maintenance, sampling, experimental analysis, statistical analysis, drafting and editing manuscript; S. Skoupý: isolation and maintenance of the cultures, experimental analysis, editing manuscript; P. Hašler: isolation and maintenance of the cultures, editing manuscript; A. Poulíčková: editing manuscript and review process; P. Dvořák: conceptualization, sampling, editing manuscript and review process.

Data availability statement

All 16S rRNA and 16S–23S ITS sequences have been deposited in GenBank under accession numbers MW742712–MW743209 and MW754714–MW755199 (see Supplementary table S1). Multiple sequence alignment, genetic distance matrix, geographic distance matrix, phylogenetic tree (Newick format), and R script for statistical analysis are archived in figshare and are available at https://doi.org/10.6084/m9.figshare.14422208.

Additional information

Funding

This research was funded by the Grant Agency of the Czech Republic (GAČR) with the grant 19-12994Y as well as by Internal Grant Agency (IGA) with the grant PrF-2022-002.