Abstract
Marine microbes are an important control on the biogeochemical cycling of trace metals, but simultaneously, these metals can control the growth of microorganisms and the cycling of major nutrients like C and N. However, studies on the response/limitation of microorganisms to trace metals have traditionally focused on the response of autotrophic phytoplankton to Fe fertilization. Few reports are available on the response of heterotrophic prokaryotes to Fe, and even less to other biogeochemically relevant metals. We performed the first study coupling dark incubations with next generation sequencing to specifically target the functional and phylogenetic response of heterotrophic prokaryotes to Fe enrichment. Furthermore, we also studied their response to Co, Mn, Ni, Zn, Cu (individually and mixed), using surface and deep samples from either coastal or open-ocean waters. Heterotrophic prokaryotic activity was stimulated by Fe in surface open–ocean, as well as in coastal, and deep open-ocean waters (where Zn also stimulated). The most susceptible populations to trace metals additions were uncultured bacteria (e.g., SAR324, SAR406, NS9, and DEV007). Interestingly, hydrocarbon-degrading bacteria (e.g., Thalassolituus, Marinobacter, and Oleibacter) benefited the most from metal addition across all waters (regions/depths) revealing a predominant role in the cycling of metals and organic matter in the ocean.
Highlights
Microbes mediate the major redox reactions responsible for transforming energy and matter in the world through enzymatic activity (Falkowski et al, 2008)
The only available study reporting on changes in heterotrophic community composition in response to trace metals by using light and dark incubations, utilized Denaturing Gradient Gel Electrophoresis (DGGE) but not generation sequencing (Jain et al, 2015). These authors found a contrasting relative decrease in Rhodospirillales in the dark relative to the light:dark cycle incubations, which further supports a strong link between phytoplankton bloom and Rhodospirillales under light incubation (Jain et al, 2015). These results indicate contrasting patterns in heterotrophic prokaryotic community composition that can be obtained when trace metal enrichment experiments are incubated under light versus dark conditions
Particulate organic carbon (POC) concentrations were similar between the shelf and slope shallow waters, particulate organic nitrogen (PON) were higher in the shelf waters (9.4 and 5.5 mg m3 at the shelf-shallow and slope-shallow, respectively), indicating a potentially richer and more labile material at the shelf
Summary
Microbes mediate the major redox reactions responsible for transforming energy and matter in the world through enzymatic activity (Falkowski et al, 2008) Many of those key enzymes contain or depend on metals, explaining why those metals are essential for life in the ocean (Morel and Price, 2003). Phytoplankton primary production is tightly linked to heterotrophic prokaryotic activity since around half of that production is remineralized through heterotrophic prokaryotes (Ducklow, 2000) These heterotrophs are competitors for limiting micronutrients such as Fe (Tortell et al, 1996; Maldonado and Price, 1999; Schmidt and Hutchins, 1999; Boyd et al, 2012). Despite this recognized tight link between primary production and heterotrophic prokaryotic activity, few investigations (see below) have tried to study the specific response of heterotrophic prokaryotes to Fe (as opposed to ‘phytoplankton mediated’ response), and even less to the other important trace metals
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