Different carboxyl‐rich alicyclic molecules proxy compounds select distinct bacterioplankton for oxidation of dissolved organic matter in the mesopelagic Sargasso Sea

Abstract

Marine dissolved organic matter (DOM) varies in its recalcitrance to rapid microbial degradation. DOM of varying recalcitrance can be exported from the ocean surface to depth by subduction or convective mixing and oxidized over months to decades in deeper seawater. Carboxyl-rich alicyclic molecules (CRAM) are characterized as a major component of recalcitrant DOM throughout the oceanic water column. The oxidation of CRAM-like compounds may depend on specific bacterioplankton lineages with oxidative enzymes capable of catabolizing complex molecular structures like long-chain aliphatics, cyclic alkanes, and carboxylic acids. To investigate the interaction between bacteria and CRAM-like compounds, we conducted microbial remineralization experiments using several compounds rich in carboxyl groups and/or alicyclic rings, including deoxycholate, humic acid, lignin, and benzoic acid, as proxies for CRAM. Mesopelagic seawater (200 m) from the northwest Sargasso Sea was used as media and inoculum and incubated over 28 d. All amendments demonstrated significant DOC removal (2-11 μmol C L −1 ) compared to controls. Bacterioplankton abundance increased significantly in the deoxycholate and benzoic acid treatments relative to controls, with fast-growing Spongiibacteracea, Euryarcheaota, and slowgrowing SAR11 enriched in the deoxycholate treatment and fast-growing Alteromonas, Euryarcheaota, and Thaumarcheaota enriched in the benzoic acid treatment. In contrast, bacterioplankton grew slower in the lignin and humic acid treatments, with oligotrophic SAR202 becoming significantly enriched in the lignin treatment. Our results indicate that the character of the CRAM proxy compounds resulted in distinct bacterioplankton removal rates of DOM and affected specific lineages of bacterioplankton capable of responding.Carboxyl-rich alicyclic molecules (CRAM), defined as a diverse array of organic compounds enriched with carboxylated and fused alicyclic rings, comprise some of the more recalcitrant compounds in the ocean (Hertkorn et al. 2006). Similar in structure to steroids and hopanoids, CRAM compounds are resistant to rapid microbial degradation (Hertkorn et al. 2006;

Pangenomics Analysis Reveals Diversification of Enzyme Families and Niche Specialization in Globally Abundant SAR202 Bacteria

“…In brainstorming these challenges, we encountered successes in confirming a pattern in DOM m/z spectra that fits one of our hypotheses (Fig. 7D), and we also identified at least one recalcitrant compound that stimulates SAR202 cell growth (36). Ongoing work in our laboratories is focused on further functional studies that test the metabolic models we propose here.…”

“…Both FMNO and RHD enzymes are powerful oxidases implicated in the catabolism of resistant compounds, such as sterols and lignins. Addition of lignin, a model recalcitrant compound, has been shown in a recent study to stimulate SAR202 growth (36). The expansion of these enzyme families is proposed to have enabled SAR202 to exploit new niches defined by these DOM resources.…”

Migratory Zooplankton Excreta and Its Influence on Prokaryotic Communities

“…To minimize sample handling and reduce the possibility of DOC contamination, this was carried out using a custom positive-pressure system that enabled subsampling without removing caps from the Biotainers. An aquarium pump pumped air through a hydrocarbon trap, which pressurized the Biotainers and displaced sample water through submerged Teflon tubing as described in Liu et al (2020). To separate copepods from the sample water, a piece of 80-µm Nytex screen was affixed to the intake end of the Teflon tube with a 1 cm piece of silicone tubing over the Nytex and Teflon tube as a collar.…”

The Role of Heterotrophic Bacteria and Archaea in the Transformation of Lignin in the Open Ocean

“…Members of the SAR202 clade of marine bacteria exhibited a maximum increase in cell abundance (Figure 5 and Supplementary Figures S2C,D) in the amended treatments at the same time when CDOM decreased. SAR202 have been estimated to account for ∼30% of all bathypelagic plankton (Morris et al, 2004;Varela et al, 2008), and studies have shown that multiple SAR202 clade genomes encode families of enzymes such as flavin-dependent monooxygenases, enolases and ring-hydroxylating dioxygenases, that may allow for the degradation of recalcitrant organic matter (Landry et al, 2017;Liu et al, 2019). As such, the ability of SAR202 to degrade lignin warrants further study.…”