Metabolism of key atmospheric volatile organic compounds by the marine heterotrophic bacterium Pelagibacter HTCC1062 (SAR11)

Abstract

Plants and phytoplankton are natural sources of the volatile organic compounds (VOCs) acetone and isoprene, which are reactive and can alter atmospheric chemistry. In earlier research we reported that, when co-cultured with a diatom, the marine bacterium Pelagibacter (strain HTCC1062; 'SAR11 clade') reduced the concentration of compounds tentatively identified as acetone and isoprene. In this study, experiments with Pelagibacter monocultures confirmed that these cells are capable of metabolizing acetone and isoprene at rates similar to bacterial communities in seawater and high enough to consume substantial fractions of the total marine acetone and isoprene budgets if extrapolated to global SAR11 populations. Homologues of an acetone/ cyclohexanone monooxygenase were identified in the HTCC1062 genome and in the genomes of a wide variety of other abundant marine taxa, and were expressed at substantial levels (c. 10 À4 of transcripts) across TARA oceans metatranscriptomes from ocean surface samples. The HTCC1062 genome lacks the canonical isoprene degradation pathway, suggesting an unknown alternative biochemical pathway is used by these cells for isoprene uptake. Fosmidomycin, an inhibitor of bacterial isoprenoid biosynthesis, blocked HTCC1062 growth, but the cells were rescued when isoprene was added to the culture, indicating SAR11 cells may be capable of synthesizing isoprenoid compounds from exogenous isoprene.

SAR11 clade microdiversity and activity during the early spring blooms off Kerguelen Island, Southern Ocean

“…Despite the differences in the environmental setting among stations (Table S1, Lasbleiz et al, 2016) the contribution of SAR11 to the total cells and to active cells appeared to be relatively constant. This is likely due to their successful adaptation to oligotrophic waters and to their capacity to efficiently take up organic substrates, among those some phytoplankton‐derived metabolites, such as very labile volatile molecules (Moore et al, 2020, 2022; Sun et al, 2011), while other taxa may favour high‐molecular‐weight DOM utilization (Malmstrom et al, 2005) as reported during the present cruise (Fourquez et al, 2016; Landa et al, 2018). So far, no known siderophores or heme uptake genes have been observed in SAR11 genomes (Hogle et al, 2016), suggesting that the success of SAR11 in these Fe‐limited waters could further be due to other specific strategies related to uptake, storage and utilization of this limiting micronutrient (Beier et al, 2015; Debeljak et al, 2019; Sun et al, 2021).…”

“…is the only subclade with Fe regulatory mechanisms for adaptation to Fe limitation (Grote et al, 2012;Smith et al, 2010). Subclade Ia is also adapted to respond to phytoplankton-derived one-carbon and volatile organic compounds (Halsey et al, 2017;Moore et al, 2020Moore et al, , 2022Sun et al, 2011). Its low requirements and efficient utilization of inorganic Fe and organic substances may explain the success of this SAR11 Ia.1 clade in the region.…”

Substantial loss of isoprene in the surface ocean due to chemical and biological consumption

“…This has been accompanied by sparse but solid evidence 20,21,34 for the presence in marine waters of isoprene-degrading bacteria belonging mainly to the phylum Actinobacteria. Two more recent studies 24,35 suggested that members of the ubiquitous SAR11, the most abundant bacterial clade in the ocean, can also consume isoprene, but this was mainly based on indirect evidence and requires confirmation. Our k loss did not show any significant correlation with the total bacterial abundance (Table 1).…”

“…Chemical oxidation is taken for granted 18 because of isoprene's high reactivity 19 , but it has never been measured. Likewise, the occurrence of isoprene-degrading bacteria in seawater has been demonstrated 20,21 and a significant microbial sink has been suggested [22][23][24] , but it has not been experimentally confirmed, let alone measured, in natural conditions including natural concentrations.…”

Identification of Volatiles of the Dinoflagellate Prorocentrum cordatum

“…In addition to vitamin transfer, symbiotic bacteria of algae can, among other tasks, take up primary metabolites from algae as dissolved organic matter (DOM) and supply inorganic nutrients [117][118][119]. It might therefore be that part of the VOCs are taken up by the bacteria in the culture as DOM [120,121], as has been shown, e.g., for the volatile isoprene [122,123]. In addition, compounds released by the bacteria and taken up by mixotrophic P. cordatum may influence the algal VOC production.…”