Open ocean and coastal strains of the N2-fixing cyanobacterium UCYN-A have distinct transcriptomes.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101285081 Publication Model: eCollection Cited Medium: Internet ISSN: 1932-6203 (Electronic) Linking ISSN: 19326203 NLM ISO Abbreviation: PLoS One Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science

Seawater*/microbiology ; Cyanobacteria*/genetics ; Cyanobacteria*/metabolism; Transcriptome ; Nitrogen Fixation/genetics ; Oceans and Seas ; Nitrogen/metabolism

Decades of research on marine N2 fixation focused on Trichodesmium, which are generally free-living cyanobacteria, but in recent years the endosymbiotic cyanobacterium Candidatus Atelocyanobacterium thalassa (UCYN-A) has received increasing attention. However, few studies have shed light on the influence of the host versus the habitat on UCYN-A N2 fixation and overall metabolism. Here we compared transcriptomes from natural populations of UCYN-A from oligotrophic open-ocean versus nutrient-rich coastal waters, using a microarray that targets the full genomes of UCYN-A1 and UCYN-A2 and known genes for UCYN-A3. We found that UCYN-A2, usually regarded as adapted to coastal environments, was transcriptionally very active in the open ocean and appeared to be less impacted by habitat change than UCYN-A1. Moreover, for genes with 24 h periodic expression we observed strong but inverse correlations among UCYN-A1, A2, and A3 to oxygen and chlorophyll, which suggests distinct host-symbiont relationships. Across habitats and sublineages, genes for N2 fixation and energy production had high transcript levels, and, intriguingly, were among the minority of genes that kept the same schedule of diel expression. This might indicate different regulatory mechanisms for genes that are critical to the symbiosis for the exchange of nitrogen for carbon from the host. Our results underscore the importance of N2 fixation in UCYN-A symbioses across habitats, with consequences for community interactions and global biogeochemical cycles.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2023 Muñoz-Marín et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

J Phycol. 2013 Dec;49(6):1024-35. (PMID: 27007623)
Nature. 2004 Aug 26;430(7003):1027-32. (PMID: 15329721)
Environ Microbiol. 2020 Jan;22(1):381-396. (PMID: 31709692)
Microbiol Rev. 1992 Jun;56(2):340-73. (PMID: 1620069)
Front Microbiol. 2017 Aug 03;8:1436. (PMID: 28824569)
Appl Environ Microbiol. 2009 Sep;75(18):6008-12. (PMID: 19633117)
Bioinformatics. 2009 Feb 1;25(3):415-6. (PMID: 19106121)
Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:327-354. (PMID: 15012266)
ISME J. 2019 Jan;13(1):170-182. (PMID: 30116043)
mBio. 2019 Jan 2;10(1):. (PMID: 30602582)
Environ Microbiol. 2019 Jan;21(1):111-124. (PMID: 30255541)
PLoS One. 2013 Dec 04;8(12):e81749. (PMID: 24324722)
Bioinformatics. 2006 Jul 1;22(13):1658-9. (PMID: 16731699)
ISME J. 2020 Oct;14(10):2395-2406. (PMID: 32523086)
Science. 2012 Sep 21;337(6101):1546-50. (PMID: 22997339)
Environ Microbiol. 2014 Oct;16(10):3238-49. (PMID: 24761991)
J Phycol. 2020 Dec;56(6):1521-1533. (PMID: 32609873)
Nat Methods. 2005 Oct;2(10):731-4. (PMID: 16179916)
Environ Microbiol. 2021 Aug;23(8):4518-4531. (PMID: 34227720)
Front Microbiol. 2021 May 05;12:666739. (PMID: 34025621)
Nucleic Acids Res. 2011 Jan;39(Database issue):D546-51. (PMID: 21045053)
Biostatistics. 2003 Apr;4(2):249-64. (PMID: 12925520)
ISME J. 2014 Jul;8(7):1476-91. (PMID: 24477198)
ISME J. 2015 Feb;9(2):273-85. (PMID: 25026373)
Physiol Plant. 2017 Nov;161(3):296-310. (PMID: 28597961)
Science. 2020 May 15;368(6492):. (PMID: 32409447)
Bioessays. 2000 Jan;22(1):10-5. (PMID: 10649285)
ISME J. 2014 Dec;8(12):2530-42. (PMID: 25226029)
Philos Trans R Soc Lond B Biol Sci. 2013 May 27;368(1621):20130121. (PMID: 23713119)
Cell Stress Chaperones. 2015 Jul;20(4):555-74. (PMID: 25986150)
Front Microbiol. 2019 Sep 24;10:2191. (PMID: 31608031)
Microbiol Mol Biol Rev. 2015 Dec;79(4):373-85. (PMID: 26335718)
FEMS Microbiol Rev. 2009 Jul;33(4):785-800. (PMID: 19416363)
Nat Commun. 2016 Mar 22;7:11071. (PMID: 27002549)
Gigascience. 2019 Jul 1;8(7):. (PMID: 31289831)
Bioinformatics. 2008 Apr 15;24(8):1063-9. (PMID: 18310054)
J Phycol. 2017 Apr;53(2):451-461. (PMID: 27992651)
Proc Natl Acad Sci U S A. 2018 Dec 26;115(52):13371-13375. (PMID: 30538206)
ISME J. 2019 Nov;13(11):2817-2833. (PMID: 31320727)
Bioinformatics. 2006 Jun 15;22(12):1540-2. (PMID: 16595560)
Appl Environ Microbiol. 2005 Sep;71(9):5362-70. (PMID: 16151126)
Nature. 2010 Mar 4;464(7285):90-4. (PMID: 20173737)
Bioinformatics. 2003 Jan 22;19(2):185-93. (PMID: 12538238)
Nat Microbiol. 2016 Dec 20;2:16214. (PMID: 27996008)
Environ Microbiol. 2015 Oct;17(10):3754-65. (PMID: 25655773)
ISME J. 2016 Mar;10(3):693-706. (PMID: 26405830)
ISME J. 2019 Feb;13(2):374-387. (PMID: 30254320)
Front Microbiol. 2018 Jul 25;9:1616. (PMID: 30090092)
Nat Microbiol. 2016 Sep 12;1(11):16163. (PMID: 27617976)

N762921K75 (Nitrogen)

Date Created: 20230502 Date Completed: 20230504 Latest Revision: 20230511

20230512

PMC10153697

10.1371/journal.pone.0272674

37130101