Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability

Shuting Liu; Nicholas Baetge; Jacqueline Comstock; Keri Opalk; Rachel Parsons; Elisa Halewood; Chance J English; Stephen Giovannoni; Luis M Bolaños; Craig E Nelson; Kevin Vergin; Craig A Carlson

doi:10.3389/fmicb.2020.580397

Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability

Front Microbiol. 2020 Oct 7:11:580397. doi: 10.3389/fmicb.2020.580397. eCollection 2020.

Affiliations

¹ Department of Ecology, Evolution, and Marine Biology, Marine Science Institute, University of California, Santa Barbara, Santa Barbara, CA, United States.
² Bermuda Institute of Ocean Sciences, Saint George, Bermuda.
³ Department of Microbiology, Oregon State University, Corvallis, OR, United States.
⁴ Daniel K. Inouye Center for Microbial Oceanography: Research and Education, Department of Oceanography and Hawai'i Sea Grant, School of Ocean and Earth Science and Technology, University of Hawai'i at Mānoa, Honolulu, HI, United States.
⁵ Microbial DNA Analytics, Phoenix, OR, United States.

Abstract

Bacterioplankton consume about half of the dissolved organic matter (DOM) produced by phytoplankton. DOM released from phytoplankton consists of a myriad of compounds that span a range of biological reactivity from labile to recalcitrant. Linking specific bacterioplankton lineages to the incorporation of DOM compounds into biomass is important to understand microbial niche partitioning. We conducted a series of DNA-stable isotope probing (SIP) experiments using ¹³C-labeled substrates of varying lability including amino acids, cyanobacteria lysate, and DOM from diatom and cyanobacteria isolates concentrated on solid phase extraction PPL columns (SPE-DOM). Amendments of substrates into Sargasso Sea bacterioplankton communities were conducted to explore microbial response and DNA-SIP was used to determine which lineages of Bacteria and Archaea were responsible for uptake and incorporation. Greater increases in bacterioplankton abundance and DOC removal were observed in incubations amended with cyanobacteria-derived lysate and amino acids compared to the SPE-DOM, suggesting that the latter retained proportionally more recalcitrant DOM compounds. DOM across a range of bioavailability was utilized by diverse prokaryotic taxa with copiotrophs becoming the most abundant ¹³C-incorporating taxa in the amino acid treatment and oligotrophs becoming the most abundant ¹³C-incorporating taxa in SPE-DOM treatments. The lineages that responded to SPE-DOM amendments were also prevalent in the mesopelagic of the Sargasso Sea, suggesting that PPL extraction of phytoplankton-derived DOM isolates compounds of ecological relevance to oligotrophic heterotrophic bacterioplankton. Our study indicates that DOM quality is an important factor controlling the diversity of the microbial community response, providing insights into the roles of different bacterioplankton in resource exploitation and efficiency of marine carbon cycling.

Keywords: DOM; Sargasso Sea; bioavailability; copiotrophs; labile; oligotrophs; recalcitrant; stable isotope probing.