Saharan dust nutrients promote Vibrio bloom formation in marine surface waters

Abstract

Vibrio is a ubiquitous genus of marine bacteria, typically comprising a small fraction of the total microbial community in surface waters, but capable of becoming a dominant taxon in response to poorly characterized factors. Iron (Fe), often restricted by limited bioavailability and low external supply, is an essential micronutrient that can limit Vibrio growth. Vibrio species have robust metabolic capabilities and an array of Fe-acquisition mechanisms, and are able to respond rapidly to nutrient influx, yet Vibrio response to environmental pulses of Fe remains uncharacterized. Here we examined the population growth of Vibrio after natural and simulated pulses of atmospherically transported Saharan dust, an important and episodic source of Fe to tropical marine waters. As a model for opportunistic bacterial heterotrophs, we demonstrated that Vibrio proliferate in response to a broad range of dust-Fe additions at rapid timescales. Within 24 h of exposure, strains of Vibrio cholerae and Vibrio alginolyticus were able to directly use Saharan dust–Fe to support rapid growth. These findings were also confirmed with in situ field studies; arrival of Saharan dust in the Caribbean and subtropical Atlantic coincided with high levels of dissolved Fe, followed by up to a 30-fold increase of culturable Vibrio over background levels within 24 h. The relative abundance of Vibrio increased from ∼1 to ∼20% of the total microbial community. This study, to our knowledge, is the first to describe Vibrio response to Saharan dust nutrients, having implications at the intersection of marine ecology, Fe biogeochemistry, and both human and environmental health.

ANaganishiain high places: functioning populations or dormant cells from the atmosphere?

“…Also, given that they are halotolerant (rather than halophilic), psychrotolerant (rather than psychrophilic), and metabolically versatile indicates that they are flexible in their response to water potential, temperature, and nutrient availability. Therefore, given the evidence available so far, our working model for why Naganishia species are so prevalent on these high elevation volcanoes is that they are flexible “opportunitrophs” ( cf Polz et al 2006; Westrich et al 2016) that can grow during rare periods of water (from melting snow) and nutrient availability (from Aeolian inputs). However, much more work is needed to verify that Naganishia species are actually functioning in these high elevation soils (and at similar sites in Antarctica) and to understand how they are dispersed through the atmosphere to remote sites throughout the cryosphere.…”

Toward a Regional Classification to Provide a More Inclusive Examination of the Ocean Biogeochemistry of Iron-Binding Ligands

“…Biologically produced Fe-binding organic ligands are (i) related to alleviation of Fe stress [bacterially-produced siderophores (Rue and Bruland, 1995;Trick et al, 1995;Mawji et al, 2008;Velasquez et al, 2011), the toxin domoic acid produced by the diatom Nitzschia Maldonado et al, 2002)], (ii) retention of episodic iron input (Adly et al, 2015;Westrich et al, 2016), or (iii) ligands produced through biological recycling or basal biological activity such as hemes , ferritin (Castruita et al, 2008), polysaccharides (Ozturk et al, 2004;Hassler et al, 2011a), and EPS (Nichols et al, 2004;Hassler et al, 2011b;Norman et al, 2015). Interestingly, amongst most of these organic ligands, only EPS were reported to contribute to the pool of HS-like substances which is not surprising given that EPS and HS are polyfunctional macromolecules.…”

“…Enhanced production of siderophores should be linked to regional patterns in heterotrophic bacterial and cyanobacteria iron stress and its opportunistic alleviation (Kirchman et al, 2009;Adly et al, 2015;Westrich et al, 2016) using a wide range of iron acquisition strategies (Cordero et al, 2012;Moran et al, 2016). Most of the insights gained into siderophores distributions have relied upon the comparable conditional stability constants between them and the L 1 class of ligands, even though no direct links have been made to date between siderophores and the L 1 class (MacRellis et al, 2001).…”

“…The observations of low concentrations (<10 pM) of siderophores (Boiteau et al, 2016a;Repeta et al, 2016) may be due to energetic constraints associated with their production (Volker and Wolf-Gladrow, 1999) and the "public goods" theory, in which synergies and multiple uptake strategies take place amongst a consortium of heterotrophic bacteria (e.g., Cordero et al, 2012). The cost of siderophores production must be traded off against the benefit obtained from the ability to rapidly sequester iron that is supplied episodically such as by dust inputs (Boyd and Tagliabue, 2015;Westrich et al, 2016). Overall, these calculations ( Figure 3A) point out that even a low concentration of siderophores is effective for bacterial uptake as they can use the bulk of Fe-L 2 complexes as a suitable exchangeable iron pool.…”

Vibrio Population Dynamics in Mid-Atlantic Surface Waters during Saharan Dust Events

“…Although perhaps best known as pathogens, of the ∼150 currently described species, only 12 are typically associated with human disease; however, all play potentially important roles in nutrient and chemical cycling in the marine environment (Grimes et al, 2009). Vibrio have a broad metabolic and genomic potential, are able to take advantage of ephemeral pulses of nutrients through chemotaxis and motility, and show rapid growth in response to nutrient addition (Worden et al, 2006;Takemura et al, 2014;Westrich et al, 2016). Vibrio are often found in close association with plankton and marine particulates where they degrade a broad range of substrates with extracellular enzymatic proteins such as chitinases, proteases, and lipases (Thompson and Polz, 2006), but can also survive in a free-living state (Worden et al, 2006;Hunt et al, 2008).…”