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Dose-Dependent Regulation of Microbial Activity on Sinking Particles by Polyunsaturated Aldehydes: Implications for the Carbon Cycle

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Dose-Dependent Regulation of Microbial Activity on Sinking Particles by Polyunsaturated Aldehydes: Implications for the Carbon Cycle Dose-dependent regulation of microbial activity on sinking particles by polyunsaturated aldehydes: Implications for the carbon cycle Bethanie R. Edwardsa,b, Kay D. Bidlec, and Benjamin A. S. Van Mooya,1 aDepartment of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543; bDepartment of Earth, Atmospheric, and Planetary Science, Massachusetts Institute of Technology, Cambridge, MA 02139; and cDepartment of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901 Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved March 24, 2015 (received for review December 1, 2014) Diatoms and other phytoplankton play a crucial role in the global interest. The stage for discovery of these molecules was set in the carbon cycle, fixing CO2 into organic carbon, which may then be 1990s, when a group of researchers advanced the “paradox of exported to depth via sinking particles. The molecular diversity of this diatom-copepod interactions”—the observation that copepods, organic carbon is vast and many highly bioactive molecules have which prey on diatoms, exhibited decreased reproductive success been identified. Polyunsaturated aldehydes (PUAs) are bioactive on when exclusively fed diatoms (6–8). Miralto et al. (9) later purified various levels of the marine food web, and yet the potential for these PUAs from diatom cultures and observed arrested embryogenesis molecules to affect the fate of organic carbon produced by diatoms of copepod eggs that were exposed to these compounds. PUA remains an open question. In this study, the effects of PUAs on the production is now a well-characterized stress surveillance response natural microbial assemblages associated with sinking particles were to wounding during grazing and to nutrient depletion, both of investigated. Sinking particles were collected from 150 m in the water column and exposed to varying concentrations of PUAs in dark in- which are bloom termination mechanisms (10, 11). cubations over 24 h. PUA doses ranging from 1 to 10 μMstimulated It has been proposed that PUAs also mediate phytoplankton respiration, organic matter hydrolysis, and cell growth by bacteria bloom dynamics by impacting other members of the marine associated with sinking particles. PUA dosages near 100 μMappeared planktonic community, aside from zooplankton. In culture con- to be toxic, resulting in decreased bacterial cell abundance and me- ditions, many eukaryotic phytoplankton experience a decrease in tabolism, as well as pronounced shifts in bacterial community com- growth rate when exposed to PUAs (12, 13). Isolated bacterial position. Sinking particles were hot spots for PUA production that strains demonstrate a varied response to PUAs, whereby diatom- contained concentrations within the stimulatory micromolar range in associated isolates are generally unaffected, whereas other strains contrast to previously reported picomolar concentrations of these exhibit either dose-dependent decreases or increases in growth compounds in bulk seawater. This suggests PUAs produced in situ rate in response to PUAs (14). Although many culture studies stimulate the remineralization of phytoplankton-derived sinking or- have been conducted on zooplankton, phytoplankton, and bac- ganic matter, decreasing carbon export efficiency, and shoaling the terial isolates—all important players in the microbial loop— average depths of nutrient regeneration. Our results are consistent there have been few attempts to study the impact of PUAs on “ ” with a bioactivity hypothesis for explaining variations in carbon these trophic levels in natural marine ecosystems under in situ export efficiency in the oceans. condition (15, 16). Surveys of water column concentrations of PUAs suggest that concentrations are generally much lower than polyunsaturated aldehydes | sinking particles | particle-associated levels required to elicit responses in phytoplankton, zooplankton, bacteria | marine carbon cycle | bioactivity hypothesis Significance EARTH, ATMOSPHERIC, lanktonic microbes in the world’s oceans play a major role in AND PLANETARY SCIENCES Pthe global carbon cycle. Through photosynthesis, phyto- plankton convert carbon dioxide into particulate organic carbon Phytoplankton live in the sunlit surface waters of the ocean, (POC), which then has the potential to sink to the deep sea. This and through photosynthesis they convert atmospherically de- process is opposed by zooplankton and heterotrophic bacteria, rived carbon dioxide into their biomass. A fraction of this which, as agents of respiration, degrade organic matter and convert biomass sinks into the darker depths where it is colonized by it back into carbon dioxide. In addition to respiring POC, hetero- bacteria that turn it back into carbon dioxide through respira- SCIENCES tion. Thus, phytoplankton–bacteria interactions effectively trophic bacteria that are associated with sinking POC use mem- ENVIRONMENTAL transport carbon dioxide from the atmosphere deep into the brane-bound ectohydrolytic enzymes that affect the disaggregation ocean. We discovered that the biomass of some phytoplankton of POC into smaller nonsinking particles and dissolved organic contains bioactive molecules that stimulate these associated carbon (DOC) (1). Despite the long-recognized role of particle- bacteria, resulting in respiration of phytoplankton biomass at associated bacteria (2), the relationships between the activities of shallower depths. Given that the ocean mixes gradually over these bacteria, particle properties, and the time and depth scales of time, carbon dioxide released by bacteria at shallower depths sinking POC degradation, disaggregation, and respiration remain returns to the surface more quickly and thereby is “seques- poorly constrained. Although the molecular-level composition of tered” from the atmosphere for a shorter duration. sinking POC has been used to identify its phytoplanktonic sources and to constrain the timescales of its degradation by heterotrophic Author contributions: B.R.E., K.D.B., and B.A.S.V.M. designed research; B.R.E. and B.A.S.V.M. bacteria (3–5), none of these studies has accounted for the potential performed research; B.R.E. and B.A.S.V.M. analyzed data; and B.R.E., K.D.B., and B.A.S.V.M. impacts of bioactive molecules within sinking POC on the activities wrote the paper. of particle-associated bacteria. The authors declare no conflict of interest. Diatoms are key members of the phytoplanktonic communi- This article is a PNAS Direct Submission. ties across the world’s ocean and are known to produce a large 1To whom correspondence should be addressed. Email: [email protected]. diversity of organic molecules, including many that are bioactive. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. Polyunsaturated aldehydes (PUAs) have received particular 1073/pnas.1422664112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1422664112 PNAS | May 12, 2015 | vol. 112 | no. 19 | 5909–5914 Downloaded by guest on September 26, 2021 or bacteria (17, 18). Consequently, the impact of PUAs on the 14 3.9 4.1 APase marine carbon cycle remains an open question. Lipase 12 Results Peptidase α-glucosidase Exposure to PUAs Affects Changes in the Rates of Sinking POC 10 Remineralization. We tested the linkages between PUAs and the rate of organic matter remineralization by particle-associated bac- 8 teria at six stations across the North Atlantic Ocean (Fig. S1 and Table S1): three stations in the Sargasso Sea (SS), two in the 6 temperate western North Atlantic (TWNA), and one in the Sub- arctic North Atlantic (SANA). Our experimental methods centered 4 1.4 vy Normalized to the Control i on collecting sinking particles, incubating particles in the presence t 1.4 0.6 ci 2 0.7 of exogenous PUAs (mixture of heptadienal, octadienal, and dec- A 0.2 adienal) at a range of concentrations, and assessing changes in or- ganic matter respiration, hydrolytic enzyme activity, bacterial cell 0 abundance, bacterial production rates, and bacterial community Enzyme structure. The absolute values of these parameters varied consid- Control 1 μM 10 μM 100 μM erably between stations (Fig. S2). To remove between-stations variability, we divided the average values of the PUA-amended Fig. 2. Average effects of PUA amendments on APase, lipase, aminopep- tidase, and α-glucosidase activity (n = 18 for all), presented as the normalized treatments by the average of the no-amendment controls from each ratio to the no-amendment control incubations. Statistical analyses con- corresponding station. These control-normalized data showed ducted as described for Fig. 1. The red values above the data report the strikingly similar responses by particle-associated bacteria to PUA average values for each treatment across all experiments and denote sta- treatments across this ocean basin (Figs. 1 and 2). We then asked tistical difference from the control, P < 0.05 (Wilcoxon rank sum). whether there were differences between the controls and the in- cubations amended with different concentrations of PUAs using a series of Wilcoxon ranked-sum statistical tests. times that of the control in the 1 and 10 μM treatments. Lipase In general, the addition of exogenous PUAs at lower con- activity was significantly lower than the control in the 100 μM centrations led to stimulated rates of bacterial organic matter treatments. Peptidase activity was significantly lower than the μ α remineralization. The average respiration rates in the 1
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