Pelagibacter metabolism of diatom‐derived volatile organic compounds imposes an energetic tax on photosynthetic carbon fixation

Abstract

Volatile organic compounds (VOCs) produced by phytoplankton are molecules with high vapor pressures that can diffuse across cell membranes into the environment, where they become public goods. VOCs likely comprise a significant component of the marine dissolved organic carbon (DOC) pool utilized by microorganisms, but they are often overlooked as growth substrates because their diffusivity imposes analytical challenges. The roles of VOCs in the growth of the photoautotrophic diatom Thalassiosira pseudonana and heterotrophic bacterium Pelagibacter sp. HTCC1062 (SAR11) were examined using co-cultures and proton-transfer reaction time-of-flight mass spectrometry. VOCs at 82 m/z values were produced in the cultures, and the concentrations of 9 of these m/z values changed in co-culture relative to the diatom monoculture. Several of the m/z values were putatively identified, and their metabolism by HTCC1062 was confirmed by measuring ATP production. Diatom carbon fixation rates in co-culture with HTCC1062 were 20.3% higher than the diatom monoculture. Removal of VOCs from the T. pseudonana monoculture using a hydrocarbon trap caused a similar increase in carbon fixation (18.1%). These results show that a wide range of VOCs are cycled in the environment, and the flux of VOCs from phytoplankton to bacterioplankton imposes a large and unexpected tax on phytoplankton photosynthesis.

The Volatilomes of Symbiodiniaceae-Associated Bacteria Are Influenced by Chemicals Derived From Their Algal Partner

“…Despite the important roles that BVOCs can play in enhancing the growth and survival of microorganisms (Stotzky and Schenck, 1976;Ryu et al, 2003Ryu et al, , 2004Ramirez et al, 2010;Schmidt et al, 2015;Moore et al, 2019), bacterial BVOC production and emission remains relatively unexplored. Numerous BVOCs have been detected from a range of bacteria and while we are currently unable to identify or determine the ecological relevance of them all, they have the potential to strongly influence the growth and success of neighboring microorganisms.…”

“…Numerous BVOCs have been detected from a range of bacteria and while we are currently unable to identify or determine the ecological relevance of them all, they have the potential to strongly influence the growth and success of neighboring microorganisms. For example, the most abundant bacterium on Earth, Pelagibacter (SAR11), metabolizes diatom derived BVOCs, which constitute a significant portion of the carbon released by phytoplankton cells (Moore et al, 2019). Furthermore, bacteria often live within or associated with a host Raina et al (2019) and as such, bacterial emissions can interact and react with host emissions (Schmidt et al, 2015;Kai et al, 2018).…”

Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts

“…While no direct evidence exists for "Ca. Fonsibacter," its similarity to the marine sister clade Pelagibacter suggests that it has overcome auxotrophic limitations by scavenging metabolites and other compounds produced by phototrophs (51). In Lake Erken, this would be primarily dying and senescent Stramenopiles as reflected in the apparent negative correlation.…”

Seasonal and Spatial Variability in the Biogenic Production and Consumption of Volatile Organic Compounds (VOCs) by Marine Plankton in the North Atlantic Ocean

“…Yet, a growing body of work provides evidence for VOC cycling between planktonic groups in the surface ocean. For example, the range of VOCs consumed by abundant chemoheterotrophic bacteria, Pelagibacter, includes methanol (Sun et al, 2011), acetaldehyde (Halsey et al, 2017), acetone, cyclopentanol, cyclohexanol, and other yet unidentified compounds (Moore et al, 2020), but Pelagibacter can also simultaneously produce the climateactive gases, dimethylsulfide (DMS) and methanethiol, through metabolism of dimethylsulfoniopropionate (DMSP) (Sun et al, 2016). Other bacterioplankton are known to utilize assortments of single-carbon compounds for energy production or, in the cases of methanol and formaldehyde, a carbon source for assimilation into biomass (i.e., growth) (Dixon et al, 2011a,b;Sun et al, 2011;Halsey et al, 2012).…”