A novel cyanobacterial geosmin producer, revising GeoA distribution and dispersion patterns in Bacteria

Abstract

cyanobacteria are ubiquitous organisms with a relevant contribution to primary production in all range of habitats. cyanobacteria are well known for their part in worldwide occurrence of aquatic blooms while producing a myriad of natural compounds, some with toxic potential, but others of high economical impact, as geosmin. We performed an environmental survey of cyanobacterial soil colonies to identify interesting metabolic pathways and adaptation strategies used by these microorganisms and isolated, sequenced and assembled the genome of a cyanobacterium that displayed a distinctive earthy/musty smell, typical of geosmin, confirmed by GC-MS analysis of the culture's volatile extract. Morphological studies pointed to a new Oscillatoriales soil ecotype confirmed by phylogenetic analysis, which we named Microcoleus asticus sp. nov. our studies of geosmin gene presence in Bacteria, revealed a scattered distribution among Cyanobacteria, Actinobacteria, Delta and Gammaproteobacteria, covering different niches. Careful analysis of the bacterial geosmin gene and gene tree suggests an ancient bacterial origin of the gene, that was probably successively lost in different time frames. The high sequence similarities in the cyanobacterial geosmin gene amidst freshwater and soil strains, reinforce the idea of an evolutionary history of geosmin, that is intimately connected to niche adaptation. Cyanobacteria can be found in marine, brackish and freshwaters exhibiting both planktonic and benthic lifestyles, covering almost all ranges of temperatures and salinities, in symbiosis with a variety of organisms, in soil, caves, deserts, and buildings, and are among the oldest life forms that evolved throughout time 1,2. It represents a prokaryotic group with huge diversity; in morphology presenting from unicellular to filamentous forms with specialized cells; chemo-diverse since they produce a panoply of bioactive compounds: antifungal 3,4 , anticancer 3,5 , antibacterial 3 , antiviral 5 , algicidal 6 , and antioxidant 7 , as well as toxic compounds noxious to the health of humans and wildlife 8,9. Two of the most common volatile organic compounds produced by Cyanobacteria are 2-Methylisoborneol (MIB, PubChem CID:16913) and Geosmin (PubChem CID:29746) 10-12. These compounds are frequently described in fresh and brackish waters Cyanobacteria, as they cause taste and odor problems in drinking water, fish and shellfish 11,13,14. Although non-toxic to humans, these compounds change the perception of safety by the public, causing major economic losses in both sectors 10,11,14. Geosmin is greatly associated with terrestrial environments. It is assumed that the organisms responsible for the gross production of geosmin in soil are Bacteria belonging to actinomycetes-Norcardia cummidelens; N. fluminea; Streptomyces Luridiscabiei; S. albidoflavus-since they are typical soil inhabitants 15,16. Other known producers of geosmin are fungi-Penicillium discolour, P. crustosum, P. expansum, Botrytis cinerea, and Chaetomium sp.-that are also present i...

The ubiquitous terpene geosmin is a warning chemical

“…Geosmin or 2-methylisoborneol was sufficient to significantly reduce the number of worms in bacterial colonies at the 2 hr, 4 hr, and 24 hr mark (Figure 2C). At 24 hrs few worms were found in bacterial colonies treated with geosmin and 2-methylisoborneol, in line with the co-occurrence of geosmin and 2-methylisoborneol biosynthetic genes in actinobacteria and cyanobacteria, but at the concentration of terpenes in our study the effect was not statistically distinct from 2-methylisoborneol or geosmin alone 10,12 .…”

“…Though chiefly a prokaryotic metabolite, geosmin is also produced by a range of fungi 6,7 , and is found in the peel of beets 8 . Geosmin production is heavily conserved 9-12 , and frequently accompanied by another odorous terpene, 2-methylisoborneol (Figure 1A) 10,13 .…”

“…Geosmin repels egg-laying Drosophila melanogaster , which has a dedicated olfactory sensory neuron for geosmin detection 14 , and attracts mosquitos and ants 8,15 , Geosmin attracts springtails to sporulating Streptomyces colonies, which then eat the bacteria and help disperse bacterial spores 16 , but this interaction would be of limited utility in aquatic environments 12 . Due to differing primary nutrient sources, life cycles, cell wall structures, predators, and symbionts the principal geosmin producers have few features in common 9,10,12 , but all produce a wealth of non-geosmin secondary metabolites 17 . Many of these bioactive compounds inhibit the growth of prokaryotes or eukaryotes 17,18 , and may be used in nature to deter competitors and predators 19-22 .…”

Algal Toxic Compounds and Their Aeroterrestrial, Airborne and other Extremophilic Producers with Attention to Soil and Plant Contamination: A Review

“…Some of them are common in different cyanoprokaryote genera (e.g., anabaenopeptins—Aps, cyanopeptolins—CPs), while others are specific to a single genus (e.g., oscillatorin in Planktothrix ( Oscillatoria ) [ 61 ] and cryptophycins—Crs in Nostoc ) [ 59 ]. Cyanoprokaryotes are also associated with production of geosmin (Geo) and 2-methylisoborneol (MIB), routinely classified among algal taste and odour compounds (TOC), which are considered non-toxic, but are harmful to humans, animals and ecosystems [ 32 , 62 , 63 ]. Due to the problems which they cause [ 32 , 63 ] and specifically to the high economic impact of Geo [ 62 ], they were included in our analysis.…”

Evaluation of Apple Root-Associated Endophytic Streptomyces pulveraceus Strain ES16 by an OSMAC-Assisted Metabolomics Approach

“…Several reports have documented the production of geosmin (1) by a plethora of microorganisms inhabiting a variety of ecological niches, including filamentous fungi, actinomycetes, cyanobacteria, and proteobacteria, to name a few (Yamada et al, 2015;Vurukonda et al, 2018;Churro et al, 2020;Melo et al, 2020). Becher et al (2020) recently unraveled this compound's central role in Streptomyces species' lifecycle since it plays a specific role as the volatile signal molecule attracting the soil arthropods Collembola (springtails) to the producer strains.…”