Ice nucleation active bacteria in precipitation are genetically diverse and nucleate ice by employing different mechanisms

Abstract

A growing body of circumstantial evidence suggests that ice nucleation active (Ice) bacteria contribute to the initiation of precipitation by heterologous freezing of super-cooled water in clouds. However, little is known about the concentration of Ice bacteria in precipitation, their genetic and phenotypic diversity, and their relationship to air mass trajectories and precipitation chemistry. In this study, 23 precipitation events were collected over 15 months in Virginia, USA. Air mass trajectories and water chemistry were determined and 33 134 isolates were screened for ice nucleation activity (INA) at -8 °C. Of 1144 isolates that tested positive during initial screening, 593 had confirmed INA at -8 °C in repeated tests. Concentrations of Ice strains in precipitation were found to range from 0 to 13 219 colony forming units per liter, with a mean of 384±147. Most Ice bacteria were identified as members of known and unknown Ice species in the Pseudomonadaceae, Enterobacteriaceae and Xanthomonadaceae families, which nucleate ice employing the well-characterized membrane-bound INA protein. Two Ice strains, however, were identified as Lysinibacillus, a Gram-positive genus not previously known to include Ice bacteria. INA of the Lysinibacillus strains is due to a nanometer-sized molecule that is heat resistant, lysozyme and proteinase resistant, and secreted. Ice bacteria and the INA mechanisms they employ are thus more diverse than expected. We discuss to what extent the concentration of culturable Ice bacteria in precipitation and the identification of a new heat-resistant biological INA mechanism support a role for Ice bacteria in the initiation of precipitation.

Forests, atmospheric water and an uncertain future: the new biology of the global water cycle

“…At a larger scale, while challenges remain (Maggioni et al 2016), satellites and models already permit the monitoring of global patterns in precipitation and wind patterns (Spracklen et al 2012). There are major research efforts looking at aerosol particles and their origins, dynamics and influences and new discoveries remain frequent (Failor et al 2017;Gu et al 2017). I expect surprises.…”

“…Ice-nucleating organisms are found in rain (Michaud et al 2014;Hara et al 2016;Failor et al 2017). Some are especially effective at promoting freezing, for example, spores of certain rust fungi (specifically, asexual urediospores) capable of long distance atmospheric transport, nucleate ice at temperatures as warm as − 4 degrees centigrade (°C) .…”

“…For example, genetic methods now permit the detection and identification of very low concentrations of airborne microbes (Hill et al 2014;Failor et al 2017). At a larger scale, while challenges remain (Maggioni et al 2016), satellites and models already permit the monitoring of global patterns in precipitation and wind patterns (Spracklen et al 2012).…”

“…Various bacteria (gram positive and negative) possess ice nucleating activity (Failor et al 2017). Certain strains of Pseudomonas syringae (plant pathogens) appear particularly effective, allowing freezing at even comparatively high temperatures (above -10°C) (Maki et al 1974;Cochet and Widehem 2000).…”

“…Methods now permit a much more detailed assessment of bacterial communities and their activities (Hill et al 2014;Failor et al 2017). The bacterial communities on the leaf surfaces of temperate forest trees include widespread generalist taxa, some which vary with time and location, and those that associate with particular tree species (Laforest-Lapointe et al 2016).…”