Co-culture and biogeography of Prochlorococcus and SAR11

Jamie W. Becker; Shane L. Hogle; Kali Rosendo; Sallie W. Chisholm

doi:10.1038/s41396-019-0365-4

Co-culture and biogeography of Prochlorococcus and SAR11

Jamie W. Becker^*
, Shane L. Hogle
, Kali Rosendo
, Sallie W. Chisholm

^*Corresponding author for this work

Environmental and Marine Biology

Research output: Contribution to journal › Article › Scientific › peer-review

78 Citations (Scopus)

Abstract

Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 10²⁸ cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 – highlighting the biogeochemical potential of these two groups.

Original language	English
Pages (from-to)	1506-1519
Number of pages	14
Journal	ISME Journal
Volume	13
Issue number	6
DOIs	https://doi.org/10.1038/s41396-019-0365-4
Publication status	Published - 1 Jun 2019
MoE publication type	A1 Journal article-refereed

Funding

Acknowledgements We thank Stephen Giovannoni and Amy Carter for preparation and shipment of SAR11 strain HTCC7211 and Jessica Berta-Thompson and Kristen LeGault for assisting in the isolation and purification of Prochlorococcus strain MIT1314. We also thank Thomas Hackl, Steven Biller, Paul Berube, Brandon Satinsky and Rogier Braakman for helpful discussions, and Ben Temperton for comments provided during the review process that significantly improved the manuscript. This work was supported in part by grants from the National Science Foundation (OCE-1153588 and DBI-0424599 to S.W.C.), the Simons Foundation (Life Sciences Project Award ID 337262, S.W.C; SCOPE Award ID 329108, S.W.C), and the Gordon and Betty Moore Foundation (Grant IDs GBMF495 and GBMF4511 to S.W.C.). This paper is a contribution from the Simons Collaboration on Ocean Processes and Ecology (SCOPE) and from the NSF Center for Microbial Oceanography: Research and Education (C-MORE).

Access to Document

10.1038/s41396-019-0365-4

Cite this

@article{13410c8a08904b63bd846f5ce11577c3,

title = "Co-culture and biogeography of Prochlorococcus and SAR11",

abstract = "Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 {\texttimes} 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15{\textendash}70\% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11{\textquoteright}s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 {\textendash} highlighting the biogeochemical potential of these two groups.",

author = "Becker, \{Jamie W.\} and Hogle, \{Shane L.\} and Kali Rosendo and Chisholm, \{Sallie W.\}",

note = "Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = jun,

day = "1",

doi = "10.1038/s41396-019-0365-4",

language = "English",

volume = "13",

pages = "1506--1519",

journal = "ISME Journal",

issn = "1751-7362",

publisher = "Springer Nature [academic journals on nature.com]",

number = "6",

}

TY - JOUR

T1 - Co-culture and biogeography of Prochlorococcus and SAR11

AU - Becker, Jamie W.

AU - Hogle, Shane L.

AU - Rosendo, Kali

AU - Chisholm, Sallie W.

PY - 2019/6/1

Y1 - 2019/6/1

N2 - Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 – highlighting the biogeochemical potential of these two groups.

AB - Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 – highlighting the biogeochemical potential of these two groups.

UR - https://www.scopus.com/pages/publications/85061397196

U2 - 10.1038/s41396-019-0365-4

DO - 10.1038/s41396-019-0365-4

M3 - Article

C2 - 30742057

AN - SCOPUS:85061397196

SN - 1751-7362

VL - 13

SP - 1506

EP - 1519

JO - ISME Journal

JF - ISME Journal

IS - 6

ER -

Co-culture and biogeography of Prochlorococcus and SAR11

Abstract

Funding

Access to Document

Other files and links

Fingerprint

Cite this