Distinct dissolved organic matter sources induce rapid transcriptional responses in coexisting populations of Prochlorococcus, Pelagibacter and the OM60 clade

Abstract

23A considerable fraction of the Earth's organic carbon exists in dissolved form in seawater. 24To investigate the roles of planktonic marine microbes in the biogeochemical cycling of 25 this dissolved organic matter (DOM), we performed controlled seawater incubation 26 experiments and followed the responses of an oligotrophic surface water microbial 27 assemblage to perturbations with DOM derived from an axenic culture of 28Prochlorococcus, or high-molecular weight DOM concentrated from nearby surface 29waters. The rapid transcriptional responses of both Prochlorococcus and Pelagibacter 30 populations suggested the utilization of organic nitrogen compounds common to both 31 DOM treatments. Along with these responses, both populations demonstrated 32 decreases in gene transcripts associated with nitrogen stress, including those involved in 33 ammonium acquisition. In contrast, responses from low abundance organisms of the 34 NOR5/OM60 gammaproteobacteria were observed later in the experiment, and 35 included elevated levels of gene transcripts associated with polysaccharide uptake and 36 oxidation. In total, these results suggest that numerically dominant oligotrophic 37 microbes rapidly acquire nitrogen from commonly available organic sources, and also 38 point to an important role for carbohydrates found within the DOM pool for sustaining 39 the less abundant microorganisms in these oligotrophic systems. 40 41

Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean

“…Nevertheless, a relatively large number of bacterial taxa in the ocean have been implicated in HWM-DOM turnover, either through experimental additions or following phytoplankton blooms, and some overlap should be expected between these taxa and those involved in HWM-DON cycling. These include the Alteromonads (for example, McCarren et al, 2010;Sharma et al, 2014;Mayali et al, 2015), Flavobacteria (for example, Kirchman, 2002;RintaKanto et al, 2012;Teeling et al, 2012;Sharma et al, 2014;Mayali et al, 2015) and the gammaproteobacterial clades NOR5/OM60, SAR92 (Teeling et al, 2012;Sharma et al, 2014) and SAR86 (Dupont et al, 2012). Bacterial groups specifically implicated in the cycling of HMW-DON and proteins include the Flavobacteria (Cottrell and Kirchman, 2000;Kirchman, 2002), the γ-Proteobacteria subgroups Arctic96B16, Ant4D3 and SAR86 (Nikrad et al, 2014), and the α-Proteobacteria clade SAR11 (Malmstrom et al, 2005).…”

Microbial cycling of marine high molecular weight dissolved organic matter

“…New insights from cultivation-independent techniques in oxygenated marine waters have gained insight into the aerobic microbial loop (McCarren et al, 2010a;Ottesen et al, 2013Rinta-Kanto, Sun, Sharma, Kiene, & Moran, 2012;Sharma et al, 2014;, wherein heterotrophic bacterioplankton play a central role in the turnover of dissolved organic matter (DOM) and serve as a link to higher trophic levels . These studies are extremely valuable because they provide information about the microbial taxa, biochemical pathways, and temporal and spatial scales that are relevant to DOM turnover, albeit they lack details illustrating the exact molecular transformations underlying the bacterial degradation of DOM substrates.…”

“…Bacteria and Archaea are the dominant degraders of DOM (Carlson, 2002), but the specific taxa, genes and molecular mechanisms most responsible for DOM metabolism remain relatively obscure. Recently, several culture-independent studies have begun to identify the microbial community members that respond to DOM enrichment, though the majority of these studies have focused on DOM isolated from phytoplankton cultures (Beier, Rivers, Moran, & Obernosterer, 2014;Landa et al, 2013;Nelson & Carlson, 2012;Poretsky, Sun, Mou, & Moran, 2010;Sarmento & Gasol, 2012;Sharma et al, 2014) which is presumed to be more labile than HMW DOM collected in oligotrophic environments. This is likely because of the presence of labile proteins and amino acids (Sarmento et al, 2013) and homopolysaccharides (Meon & Kirchman, 2001) in phytoplankton DOM.…”

“…Aluwihare & Repeta (1999) and observed rapid drawdown of phytoplankton DOM and evolution of polysaccharides from homopolysaccharides (energy storage products) to heteropolysaccharides with a composition like HMW DOM. In contrast, there have been fewer culture-independent studies focusing on the cycling of HMW DOM (McCarren et al, 2010b;Sharma et al, 2014). In all of these studies, DOM additions resulted in the enrichment of select members of the microbial community and in several cases a temporal succession of DOM-degrading bacteria (McCarren et al, 2010b;Sharma et al, 2014).…”

“…In contrast, there have been fewer culture-independent studies focusing on the cycling of HMW DOM (McCarren et al, 2010b;Sharma et al, 2014). In all of these studies, DOM additions resulted in the enrichment of select members of the microbial community and in several cases a temporal succession of DOM-degrading bacteria (McCarren et al, 2010b;Sharma et al, 2014).…”