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Spatially structured bacterial interactions alter algal carbon flow to bacteria

Journal Article · · The ISME Journal
Phytoplankton account for nearly half of global photosynthetic carbon fixation, and the fate of that carbon is regulated in large part by microbial food web processing. We currently lack a mechanistic understanding of how interactions among heterotrophic bacteria impact the fate of photosynthetically fixed carbon. Here, we used a set of bacterial isolates capable of growing on exudates from the diatom Phaeodactylum tricornutum to investigate how bacteria-bacteria interactions affect the balance between exudate remineralization and incorporation into biomass. With exometabolomics and genome-scale metabolic modeling, we estimated the degree of resource competition between bacterial pairs. In a sequential spent media experiment, we found that pairwise interactions were more beneficial than predicted based on resource competition alone, and 30% exhibited facilitative interactions. To link this to carbon fate, we used single-cell isotope tracing in a custom cultivation system to compare the impact of different "primary" bacterial strains in close proximity to live P. tricornutum on a distal "secondary" strain. We found that a primary strain with a high degree of competition decreased secondary strain carbon drawdown by 51% at the single-cell level, providing a quantitative metric for the "cost" of competition on algal carbon fate. Additionally, a primary strain classified as facilitative based on sequential interactions increased total algal-derived carbon assimilation by 7.6 times, integrated over all members, compared to the competitive primary strain. Our findings suggest that the degree of interaction between bacteria along a spectrum from competitive to facilitative is directly linked to algal carbon drawdown.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
Joint Genome Institute (JGI); US Department of Energy; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Biological Systems Science Division (SC-23.2 ); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)
Grant/Contract Number:
AC02-05CH11231; AC05-76RL01830; AC52-07NA27344
OSTI ID:
2571814
Alternate ID(s):
OSTI ID: 2575078
OSTI ID: 2584423
Report Number(s):
LLNL--JRNL-865561; PNNL-SA--204208; ark:/13030/qt4nn4b2fd; https://escholarship.org/uc/item/4nn4b2fd
Journal Information:
The ISME Journal, Journal Name: The ISME Journal Journal Issue: 1 Vol. 19
Country of Publication:
United States
Language:
English