title: Phytoplankton-bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge.
abstract: Southern Ocean primary productivity plays a key role in global ocean biogeochemistry and climate. At the Southern Ocean sea ice edge in coastal McMurdo Sound, we observed simultaneous cobalamin and iron limitation of surface water phytoplankton communities in late Austral summer. Cobalamin is produced only by bacteria and archaea, suggesting phytoplankton-bacterial interactions must play a role in this limitation. To characterize these interactions and investigate the molecular basis of multiple nutrient limitation, we examined transitions in global gene expression over short time scales, induced by shifts in micronutrient availability. Diatoms, the dominant primary producers, exhibited transcriptional patterns indicative of co-occurring iron and cobalamin deprivation. The major contributor to cobalamin biosynthesis gene expression was a gammaproteobacterial population, Oceanospirillaceae ASP10-02a. This group also contributed significantly to metagenomic cobalamin biosynthesis gene abundance throughout Southern Ocean surface waters. Oceanospirillaceae ASP10-02a displayed elevated expression of organic matter acquisition and cell surface attachment-related genes, consistent with a mutualistic relationship in which they are dependent on phytoplankton growth to fuel cobalamin production. Separate bacterial groups, including Methylophaga, appeared to rely on phytoplankton for carbon and energy sources, but displayed gene expression patterns consistent with iron and cobalamin deprivation. This suggests they also compete with phytoplankton and are important cobalamin consumers. Expression patterns of siderophore- related genes offer evidence for bacterial influences on iron availability as well. The nature and degree of this episodic colimitation appear to be mediated by a series of phytoplankton-bacterial interactions in both positive and negative feedback loops.
authors.affiliation: Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037; Integrative Oceanography Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92037;
authors.forename: Erin M
authors.initials: EM
authors.lastname: Bertrand
authors.affiliation: Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037;
authors.forename: John P
authors.initials: JP
authors.lastname: McCrow
authors.affiliation: Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037; Integrative Oceanography Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92037; Department of Biology and Biotechnology Graduate Program, American University in Cairo, Cairo, Egypt 11835;
authors.forename: Ahmed
authors.initials: A
authors.lastname: Moustafa
authors.affiliation: Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037;
authors.forename: Hong
authors.initials: H
authors.lastname: Zheng
authors.affiliation: Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037; Integrative Oceanography Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92037;
authors.forename: Jeffrey B
authors.initials: JB
authors.lastname: McQuaid
authors.affiliation: Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543;
authors.forename: Tom O
authors.initials: TO
authors.lastname: Delmont
authors.affiliation: Graduate School of Oceanography, University of Rhode Island, Narragansett, RI 02882;
authors.forename: Anton F
authors.initials: AF
authors.lastname: Post
authors.affiliation: Department of Physical Sciences, Virginia Institute of Marine Science, Gloucester Point, VA 23062;
authors.forename: Rachel E
authors.initials: RE
authors.lastname: Sipler
authors.affiliation: Department of Physical Sciences, Virginia Institute of Marine Science, Gloucester Point, VA 23062;
authors.forename: Jenna L
authors.initials: JL
authors.lastname: Spackeen
authors.affiliation: Marine and Environmental Biology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089.
authors.forename: Kai
authors.initials: K
authors.lastname: Xu
authors.affiliation: Department of Physical Sciences, Virginia Institute of Marine Science, Gloucester Point, VA 23062;
authors.forename: Deborah A
authors.initials: DA
authors.lastname: Bronk
authors.affiliation: Marine and Environmental Biology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089.
authors.forename: David A
authors.initials: DA
authors.lastname: Hutchins
authors.affiliation: Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037; Integrative Oceanography Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92037; aallen@jcvi.org.
authors.forename: Andrew E
authors.initials: AE
authors.lastname: Allen
mesh_terms: D000864:Antarctic Regions; D001419:Bacteria / Q000187:drug effects / Q000378:metabolism*; D002734:Chlorophyll / Q000378:metabolism; D000077194:Chlorophyll A; D017753:Ecosystem; D025461:Feedback, Physiological / Q000187:drug effects; D046448:Ice Cover; D007501:Iron / Q000494:pharmacology; D056265:Microbial Interactions / Q000187:drug effects; D018977:Micronutrients / Q000378:metabolism*; D016366:Open Reading Frames / Q000235:genetics; D010839:Phytoplankton / Q000187:drug effects / Q000378:metabolism*; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D013312:Stress, Physiological / Q000187:drug effects; D014805:Vitamin B 12 / Q000494:pharmacology
chemical_list: D018977:Micronutrients; D012333:RNA, Messenger; D002734:Chlorophyll; D007501:Iron; D014805:Vitamin B 12; D000077194:Chlorophyll A
keywords: Southern Ocean primary productivity; cobalamin; colimitation; metatranscriptomics; phytoplankton–bacterial interactions