Traits determine dispersal and colonization abilities of microbes

Abstract

Many microbes disperse through the air, yet the phenotypic traits that enhance or constrain aerial dispersal or allow successful colonization of new habitats are poorly understood. We used a metabarcoding bacterial and eukaryotic data set to explore the trait structures of the aquatic, terrestrial, and airborne microbial communities near the Salton Sea, California, as well as those colonizing a series of experimental aquatic mesocosms. We assigned taxonomic identities to amplicon sequence variants (ASVs) and matched them to functional trait values through published papers and databases that infer phenotypic and/or metabolic traits information from taxonomy. We asked what traits distinguish successful microbial dispersers and/or colonizers from terrestrial and aquatic source communities. Our study found broad differences in taxonomic and trait composition between dispersers and colonizers compared to the source soil and water communities. Dispersers were characterized by larger cell diameters, colony formation, and fermentation abilities, while colonizers tended to be phototrophs that form mucilage and have siliceous coverings. Shorter population doubling times, spore-, and/or cyst-forming organisms were more abundant among the dispersers and colonizers than the sources. These results show that the capacity for aerial dispersal and colonization varies among microbial functional groups and taxa and is related to traits that affect other functions like resource acquisition, predator avoidance, and reproduction. The ability to disperse and colonize new habitats may therefore distinguish microbial guilds based on tradeoffs among alternate ecological strategies.IMPORTANCEMicrobes have long been thought to disperse rapidly across biogeographic barriers; however, whether dispersal or colonization vary among taxa or groups or is related to cellular traits remains unknown. We use a novel approach to understand how microorganisms disperse and establish themselves in different environments by looking at their traits (physiology, morphology, life history, and behavior characteristics). By collecting samples from habitats including water, soil, and the air and colonizing experimental tanks, we found dispersal and invasion vary among microorganisms. Some taxa and functional groups are found more often in the air or colonizing aquatic environments, while others that are commonly found in the soil or water rarely disperse or invade new habitat. Interestingly, the traits that help microorganisms survive and thrive also play a role in their ability to disperse and colonize. These findings have significant implications for understanding microorganisms' success and adaptation to new environments.

Keywords: aerosols; airborne; community assembly; trait tradeoff.

Fig 1

Geographic location and characterization of sampling sites. (a) General overview of the geographic location, circles represent detailed spatial location of samples collected from the Salton Sea. Sampling dates are indicated by color: white = 15 January 2019 (n = 6), orange = 30 January 2019 (n = 2), pink = 17 May 2019 (n = 11), red = 27 June 2019 (n = 1), and purple = 10 July 2019 (n = 1). Inset (red rectangle) in (a) shows the location of the sampling area in (b) where (c) Environmental water samples in light blue circles and (d) Soil samples in brown circles were collected at each environment. Inset (blue rectangle) in (b) shows the sampling area inside Viridos facility in (e) where aerosol (in orange) and open colonizing tanks (in green) samples were collected. Open colonizing tanks were located in concentric rings 100 m, 200 m, 365 m, and 550 m apart. Geographic maps in (a–d) were obtained from Google Maps and (e) was obtained from Google Earth Pro.

Fig 2

Analysis of the richness and diversity of each environment type. (a) Venn diagram of shared and unique ASV numbers among samples. Shannon diversity of bacterial (b) and eukaryotic ASVs (c) by environment, respectively. Letters A, B, and C in (b) and (c) denote statistically significant differences (ANOVA; Tukey’s HSD Test P < 0.05) in Shannon’s diversity values among the compared environments.

Fig 3

Bacterial community characterization by environment type. (a) Radar plots of most abundant taxonomic groups. Groups further from the center have higher relative abundances. Only taxonomic groups above 10% relative abundance are shown. Bacterial PCoA based on (b) taxonomic composition at the ASV level. (c) Madin et al. (21) phenotypic trait database and (d) FAPROTAX functional trait database. Arrows length for cell length in (c) and aerobic chemoheterotrophy and cyano/chloroplast in (d) were reduced by a factor of 10 to help visualize all arrows on one graph. Only the top 10 ASVs are shown on the ordination in (b) represented by letters: A, J: Cyanobacteria; Family IX; GpIX, B: Cyanobacteria; Family X; GpX, C: Alphaproteobacteria; Rhodobacterales; Roseivivax, D: Actinobacteria; Actinomycetales; Corynebacterium, E: Firmicutes; Bacillales; Salinicoccus, F: Betaproteobacteria; Burkholderiales; Variovorax, G: Actinobacteria; Actinomycetales; Kocuria, H: Bacteroidetes; Sphingobacteriales; Gracilimonas, I: Alphaproteobacteria; SAR11; Candidatus Pelagibacter. Letter D is located behind E on the plot. Results from PERMANOVA (function “adonis”) statistical test in (b–d) are: Pseudo F-ratio, their associated P-value, and the R². Aer chemoHT, aerobic chemoheterotrophy; cyano/chloro, cyanobacteria/chloroplast; dia, diameter; Ferment, fermentation; HC degrad, hydrocarbon degradation; Mesoph, mesophilic; PHt, photoheterotrophy; PT, phototrophy; Spor, Sporulation; tol, tolerant.

Fig 4

Eukaryote community characterization by environment type. (a) Radar plots of most abundant taxonomic groups. Groups further from the center have higher relative abundances. Only taxonomic groups above 10% relative abundance are shown. PCoA based on (b) taxa composition at the ASV level and (c) phenotypic traits. Results from PERMANOVA (function “adonis”) statistical test in (b and c) are Pseudo F-ratio, their associated P-value, and the R². At, autotrophy; Col, colony forming; Fla, flagella; Ht, Heterotrophy; Micro, micro size; Nano, nano size; Nk, naked cover; Org, organic cover; Si, siliceous cover; Swim, swimmer.

Fig 5

Examples of phenotypic traits that differed by environment types for (a) bacteria and (b) eukaryotes. Letters A, B, C, and D denote statistically significant differences among environments (ANOVA; Tukey’s HSD Test P < 0.05). For each of the microbial communities, black circles represent samples, and red dots represent the mean. In (a), the y axis represents abundance-weighted averages of a trait in each of the samples; this is accounting for the trait value multiplied by its relative abundance; in (b), the y axis represents relative abundances of that trait in each of the samples.

Fig 6

Typology of eukaryotic functional traits, modified from Litchman and Klausmeier (42) with permission.