Jet-Suspended, Calcite-Ballasted Cyanobacterial Waterwarts in a Desert Spring

We describe a population of colonial cyanobacteria (waterwarts) that develops as the dominant primary producer in a bottom-fed, warm spring in the Cuatro Cienegas karstic region of the Mexican Chihuahuan Desert. The centimeter-sized waterwarts were suspended within a central, conically shaped, 6-m deep well by upwelling waters. Waterwarts were built by an unicellular cyanobacterium and supported a community of epiphytic filamentous cyanobacteria and diatoms but were free of heterotrophic bacteria inside. Sequence analysis of genes revealed that this cyanobacterium is only distantly related to several strains of other unicellular teria Cyanothece, Waterwarts contained orderly arrangements of mineral made up of microcrystalline low-magnesium calcite with high levels of strontium and sulfur. Waterwarts were 95.9% (v/v) glycan, 2.8% cells, and 1.3% mineral grains and had a buoyant density of 1.034 kg/L. An analysis of the hydrological properties of the spring well and the waterwarts demonstrated that both large colony size and the presence of controlled amounts of mineral ballast are required to prevent the population from being washed out of the well. The unique hydrological characteristics of the spring have likely selected for both traits. The mechanisms by which controlled nucleation of extracellular calcite is achieved remain to be explored

A comparative genomics approach to understanding the biosynthesis of the sunscreen scytonemin in cyanobacteria

BACKGROUND: The extracellular sunscreen scytonemin is the most common and widespread indole-alkaloid among cyanobacteria. Previous research using the cyanobacterium Nostoc punctiforme ATCC 29133 revealed a unique 18-gene cluster (NpR1276 to NpR1259 in the N. punctiforme genome) involved in the biosynthesis ofscytonemin. We provide further genomic characterization of these genes in N. punctiforme and extend it to homologous regions in other cyanobacteria. RESULTS: Six putative genes in the scytonemin gene cluster (NpR1276 to NpR1271 in the N. punctiforme genome), with no previously known protein function and annotated in this study as scyA to scyF, are likely involved in the assembly of scytonemin from central metabolites, based on genetic, biochemical, and sequence similarity evidence. Also in this cluster are redundant copies of genes encoding for aromatic amino acid biosynthetic enzymes. These can theoretically lead to tryptophan and the tyrosine precursor, p-hydroxyphenylpyruvate, (expected biosynthetic precursors of scytonemin) from end products of the shikimic acid pathway. Redundant copies of the genes coding for the key regulatory and rate-limiting enzymes of the shikimic acid pathway are found there as well. We identified four other cyanobacterial strains containing orthologues of all of these genes, three of them by database searches (Lyngbya PCC 8106, Anabaena PCC 7120, and Nodularia CCY 9414) and one by targeted sequencing (Chlorogloeopsis sp. strain Cgs-089; CCMEE 5094). Genomic comparisons revealed that mostscytonemin-related genes were highly conserved among strains and that two additional conserved clusters, NpF5232 to NpF5236 and a putative two-component regulatory system (NpF1278 and NpF1277), are likely involved in scytonemin biosynthesis and regulation, respectively, on the basis of conservation and location. Since many of the protein product sequences for the newly described genes, including ScyD, ScyE, and ScyF, have export signal domains, while others have putative transmembrane domains, it can be inferred that scytonemin biosynthesis is compartmentalized within the cell. Basic structural monomer synthesis and initial condensation are most likely cytoplasmic, while later reactions are predicted to be periplasmic. CONCLUSION: We show that scytonemin biosynthetic genes are highly conserved among evolutionarily diverse strains, likely include more genes than previously determined, and are predicted to involve compartmentalization of the biosynthetic pathway in the cell, an unusual trait for prokaryotes

The Evolution of a Capacity to Build Supra-Cellular Ropes Enabled Filamentous Cyanobacteria to Colonize Highly Erodible Substrates

Several motile, filamentous cyanobacteria display the ability to self-assemble into tightly woven or twisted groups of filaments that form macroscopic yarns or ropes, and that are often centimeters long and 50-200 microm in diameter. Traditionally, this trait has been the basis for taxonomic definition of several genera, notably Microcoleus and Hydrocoleum, but the trait has not been associated with any plausible function.Through the use of phylogenetic reconstruction, we demonstrate that pedigreed, rope-building cyanobacteria from various habitats do not form a monophyletic group. This is consistent with the hypothesis that rope-building ability was fixed independently in several discrete clades, likely through processes of convergent evolution or lateral transfer. Because rope-building cyanobacteria share the ability to colonize geologically unstable sedimentary substrates, such as subtidal and intertidal marine sediments and non-vegetated soils, it is also likely that this supracellular differentiation capacity imparts a particular fitness advantage in such habitats. The physics of sediment and soil erosion in fact predict that threads in the 50-200 microm size range will attain optimal characteristics to stabilize such substrates on contact.Rope building is a supracellular morphological adaptation in filamentous cyanobacteria that allows them to colonize physically unstable sedimentary environments, and to act as successful pioneers in the biostabilization process

Biological Soil Crusts as Modern Analogues for the Archean Continental Biosphere: Insights from Carbon and Nitrogen Isotopes

5 pagesInternational audienceStable isotope signatures of elements related to life such as carbon and nitrogen can be powerful biomarkers that provide key information on the biological origin of organic remains and their paleoenvironments. Marked advances have been achieved in the last decade in our understanding of the coupled evolution of biological carbon and nitrogen cycling and the chemical evolution of the early Earth thanks, in part, to isotopic signatures preserved in fossilized microbial mats and organic matter of marine origin. However, the geologic record of the early continental biosphere, as well as its evolution and biosignatures, is still poorly constrained. Following a recent report of direct fossil evidence of life on land at 3.22 Ga, we compare here the carbon and nitrogen isotopic signals of this continental Archean biosphere with biosignatures of cyanobacteria biological soil crusts (cyanoBSCs) colonizing modern arid environments. We report the first extended δ13C and δ15N data set from modern cyanoBSCs and show that these modern communities harbor specific isotopic biosignatures that compare well with continental Archean organic remains. We therefore suggest that cyanoBSCs are likely relevant analogs for the earliest continental ecosystems. As such, they can provide key information on the timing, extent, and possibly mechanism of colonization of the early Earth's emergent landmasses

The Trait Repertoire Enabling Cyanobacteria to Bloom Assessed through Comparative Genomic Complexity and Metatranscriptomics

Water bloom development due to eutrophication constitutes a case of niche specialization among planktonic cyanobacteria, but the genomic repertoire allowing bloom formation in only some species has not been fully characterized. We posited that the habitat relevance of a trait begets its underlying genomic complexity, so that traits within the repertoire would be differentially more complex in species successfully thriving in that habitat than in close species that cannot. To test this for the case of bloom-forming cyanobacteria, we curated 17 potentially relevant query metabolic pathways and five core pathways selected according to existing ecophysiological literature. The available 113 genomes were split into those of blooming (45) or nonblooming (68) strains, and an index of genomic complexity for each strain’s version of each pathway was derived. We show that strain versions of all query pathways were significantly more complex in bloomers, with complexity in fact correlating positively with strain blooming incidence in 14 of those pathways. Five core pathways, relevant everywhere, showed no differential complexity or correlations. Gas vesicle, toxin and fatty acid synthesis, amino acid uptake, and C, N, and S acquisition systems were most strikingly relevant in the blooming repertoire. Further, we validated our findings using metagenomic gene expression analyses of blooming and non- blooming cyanobacteria in natural settings, where pathways in the repertoire were differentially overexpressed according to their relative complexity in bloomers, but not in nonbloomers. We expect that this approach may find applications to other habitats and organismal groups

The compositionally distinct cyanobacterial biocrusts from brazilian savanna and their environmental drivers of community diversity

Machado de Lima, Náthali Maria. São Paulo State University (UNESP). Microbiology Graduation Program. Department of Zoology and Botany. São Paulo, Brazil.Cámara Fernandes, Vanessa Moreira. Arizona State University. Center for Fundamental and Applied Microbiomics. Biodesign Institute. Tempe, Arizona, United States.Roush, Daniel. Arizona State University. Center for Fundamental and Applied Microbiomics. Biodesign Institute. Tempe, Arizona, United States.Velasco Ayuso, Sergio. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura (IFEVA). Buenos Aires, Argentina.Rigonato, Janaina. University of São Paulo (USP). Center for Nuclear Energy in Agriculture (CENA). Piracicaba, Brazil.Garcia Pichel, Ferran. Arizona State University. Center for Fundamental and Applied Microbiomics. Biodesign Institute. Tempe, Arizona, United States.Zanini Branco, Luis Henrique. São Paulo State University (UNESP). Microbiology Graduation Program. Department of Zoology and Botany. São Paulo, Brazil.10The last decade was marked by efforts to define and identify the main cyanobacterial players in biological crusts around the world. However, not much is known about biocrusts in Brazil’s tropical savanna (cerrado), despite the existence of environments favorable to their development and ecological relevance. We examined the community composition of cyanobacteria in biocrusts from six sites distributed in the Southeast of the country using high throughput sequencing of 16S rRNA and phylogenetic placement in the wider context of biocrusts from deserts. Sequences ascribable to 22 genera of cyanobacteria were identified. Although a significant proportion of sequences did not match those of known cyanobacteria, several clades of Leptolyngbya and Porphyrosiphon were found to be the most abundant. We identified significant differences in dominance and overall composition among the cerrado sites, much larger than within-site variability. The composition of cerrado cyanobacterial communities was distinct from those known in biocrusts from North American deserts. Among several environmental drivers considered, the opposing trend of annual precipitation and mean annual temperature best explained the variability in community composition within Brazilian biocrusts. Their compositional uniqueness speaks of the need for dedicated efforts to study the ecophysiology of tropical savanna biocrust and their roles in ecosystem function for management and preservation

Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics

Microbial biosynthetic gene clusters (BGCs) encoding secondary metabolites are thought to impact a plethora of biologically mediated environmental processes, yet their discovery and functional characterization in natural microbiomes remains challenging. Here we describe deep long-read sequencing and assembly of metagenomes from biological soil crusts, a group of soil communities that are rich in BGCs. Taking advantage of the unusually long assemblies produced by this approach, we recovered nearly 3,000 BGCs for analysis, including 712 full-length BGCs. Functional exploration through metatranscriptome analysis of a 3-day wetting experiment uncovered phylum-specific BGC expression upon activation from dormancy, elucidating distinct roles and complex phylogenetic and temporal dynamics in wetting processes. For example, a pronounced increase in BGC transcription occurs at night primarily in cyanobacteria, implicating BGCs in nutrient scavenging roles and niche competition. Taken together, our results demonstrate that long-read metagenomic sequencing combined with metatranscriptomic analysis provides a direct view into the functional dynamics of BGCs in environmental processes and suggests a central role of secondary metabolites in maintaining phylogenetically conserved niches within biocrusts.Supplementary Data 1 : Description: Raw metagenome and metatranscriptome statistics.Supplementary Data 2 : Description: Assembly statistics of short- and long-read metagenomes as well as metatranscriptomes.Supplementary Data 3 : Description: Each biosynthetic gene cluster identified from the assembled metagenomes in this study.Supplementary Data 4 : Description: Each biosynthetic gene cluster identified in the metatranscriptomic assemblies.Supplementary Data 5 : Description: The genes used to calculate transcription of biosynthetic gene clusters and core bacterial genes.Supplementary Data 6 : Description: DESeq2 analysis of significantly transcribed genes between day and night-time transcription.Supplementary Data 7 : Description: Transcriptional scores for cation-related genes.Supplementary Data 8 : Description: Average abundance pattern for each phylum through time.Supplementary Data 9 : Description: Taxonomic composition of metagenomes and metatranscriptomes using fulllength 16S rRNA.Supplementary Data 10 : Description: Normalized sequence data showing scores of transcription at each time point with BGC type and Phylum shownThis work was partially supported by funds provided by the Office of Science Early Career Research Program Office of Biological and Environmental Research, of the U.S. Department of Energy and by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231 to Lawrence Berkeley National Laboratory. We also wish to acknowledge Simon Roux, Emiley Eloe-Fadrosh and Eoin Brodie for their constructive feedback.https://www.nature.com/commsbioam2022BiochemistryGeneticsMicrobiology and Plant Patholog