Biological Ice-Nucleating Particles Deposited Year-Round in Subtropical Precipitation

Abstract

Airborne bacteria that nucleate ice at relatively warm temperatures (>-10°C) can interact with cloud water droplets, affecting the formation of ice in clouds and the residency time of the cells in the atmosphere. We sampled 65 precipitation events in southeastern Louisiana over 2 years to examine the effect of season, meteorological conditions, storm type, and ecoregion source on the concentration and type of ice-nucleating particles (INPs) deposited. INPs sensitive to heat treatment were inferred to be biological in origin, and the highest concentrations of biological INPs (∼16,000 INPs liter^-1 active at ≥-10°C) were observed in snow and sleet samples from wintertime nimbostratus clouds with cloud top temperatures as warm as -7°C. Statistical analysis revealed three temperature classes of biological INPs (INPs active from -5 to -10°C, -11 to -12°C, and -13 to -14°C) and one temperature class of INPs that were sensitive to lysozyme (i.e., bacterial INPs, active from -5 to -10°C). Significant correlations between the INP data and abundances of taxa in the Bacteroidetes, Firmicutes, and unclassified bacterial divisions implied that certain members of these phyla may possess the ice nucleation phenotype. The interrelation between the INP classes and fluorescent dissolved organic matter, major ion concentrations (Na⁺, Cl^-, SO₄^2-, and NO₃^-), and backward air mass trajectories indicated that the highest concentrations of INPs were sourced from high-latitude North American and Asian continental environments, whereas the lowest values were observed when air was sourced from marine ecoregions. The intra- and extracontinental regions identified as sources of biological INPs in precipitation deposited in the southeastern United States suggests that these bioaerosols can disperse and affect meteorological conditions thousands of kilometers from their terrestrial points of origin.IMPORTANCE The particles most effective at inducing the freezing of water in the atmosphere are microbiological in origin; however, information on the species harboring this phenotype, their environmental distribution, and ecological sources are very limited. Analysis of precipitation collected over 2 years in Louisiana showed that INPs active at the warmest temperatures were sourced from terrestrial ecosystems and displayed behaviors that implicated specific bacterial taxa as the source of the ice nucleation activity. The abundance of biological INPs was highest in precipitation from winter storms and implied that their in-cloud concentrations were sufficient to affect the formation of ice and precipitation in nimbostratus clouds.

Keywords: aeromicrobiology; bacteria; biological ice nuclei; environmental microbiology; meteorology; microbial ecology; precipitation.

FIG 1

Concentrations of total, biological, and bacterial ice-nucleating particles (INPs) at activation temperatures of –4 to –15°C. The median and 95% confidence interval (CI) values are depicted by the black horizontal lines and dashed vertical lines, respectively; boxes represent the interquartile range; whiskers represent maximum and minimum values, excluding outliers; and open circles represent outliers. (a) Differential total INP concentrations, with sample sizes as follows: −4 to −12°C, n = 61; −13°C, n = 56; −14°C, n = 48; and −15°C, n = 44. (b) Differential biological INP concentrations, with sample sizes as follows: −4 to −12°C, n = 61; −13°C, n = 56; −14°C, n = 48; and −15°C, n = 44. (c) Differential bacterial INP concentrations, with sample sizes as follows: −4 to −12°C, n = 54; −13°C, n = 44; −14°C, n = 37; and −15°C, n = 34. (d) Cumulative concentrations of INPs active at temperatures of ≥−15°C for total, biological, and bacterial INPs.

FIG 2

Results of fluorescent dissolved organic matter (DOM) excitation-emission matrices data investigated using parallel factor (PARAFAC) analysis. (a to c) The three fluorescent DOM PARAFAC components (component 1 [more complex, humic-like materials] [a], component 2 [tyrosine- and tannin-like materials] [b], and component 3 [tryptophan-like materials] [c]) identified in 43 Louisiana precipitation events from 2013 to 2015 are consistent with DOM from terrestrial and aquatic environments.

FIG 3

Average INP factor concentrations as a function of ecoregion classification. Multivariate analysis of variance indicated that average INP concentrations differed based on the interactions of air masses with the various ecoregions. This plot is showing the average of summed differential INP concentrations (y axis) for each INP factor for each ecoregion. For example, bac (–5 to −10) is the average value of the summed differential INP concentrations at −5, –6, –7, –8, –9, and –10°C for each ecoregion.

FIG 4

Location and extent of the source ecoregions relevant in this study. These ecoregions of North America were defined by the EPA, USGS, and CEC, as described in the text. The source ecoregion was used to classify interaction patterns between backwards air mass trajectories and the mixed boundary layer for each precipitation event (Fig. S1). Location of the primary sampling site (Baton Rouge, LA) is indicated by the red star. EA, eastern Asia; PM, Pacific maritime; NFM, northwest forested mountains; HNL, high northern latitudes; DSAH, desert and semiarid highlands; GP, Great Plains; EWW, eastern woodlands and wetlands; NAM, North Atlantic maritime; SAM, South Atlantic maritime.

FIG 5

Average INP factor concentrations as a function of cloud type, season, and precipitation phase. (a to c) Multivariate analysis of variance indicated that average INP concentrations (Conc.) differed based on the cloud type (a), season (b), and precipitation type (c). The average of summed differential (Diff.) INP concentrations were determined as described in the Fig. 3 legend.

FIG 6

Summary of trends in ice-nucleating particle (INP) data with source ecoregion and physical, chemical, and microbiological properties of the precipitation. Ecoregions as depicted in Fig. 4 are outlined by black solid lines. (a) Key for INP concentrations in the ecoregion for panels b to g and Pearson correlation coefficents for panel h are shown. (b to g) Ecoregions that correlated significantly with total_{−5 to −11} (b), total_{−11 to −14} (c), bio_{−5 to −10} (d), bio_{−11 to −12} (e), bio_{−13 to −14} (f), and bac_{−5 to −10} (g) INP concentrations are shown. (h) Heat plot of Pearson correlation coefficients between INP concentrations and various precipitation measurements, as follows (units): cell abundance (cells liter⁻¹ precipitation); conductivity (cond.; μS cm⁻¹); chloride, sodium, nitrate, and sulfate (μM); DOC, dissolved organic carbon (parts per million); C1, PARAFAC component C1 (Raman units [R.U.]); C2, PARAFAC component C2 (A.U.); and C3, PARAFAC component C3 (A.U.).