Home LiteratureArticle Details
PMID: 21883799 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Microbial rhodopsins on leaf surfaces of terrestrial plants.

Environmental microbiology ·Vol. 14 ·No. 1 ·2012-01-00 ·Pages 140-6

Atamna-Ismaeel N, Finkel OM, Glaser F, Sharon I, Schneider R, Post AF, Spudich JL, von Mering C, Vorholt JA, Iluz D, Béjà O, Belkin S

Abstract

The above-ground surfaces of terrestrial plants, the phyllosphere, comprise the main interface between the terrestrial biosphere and solar radiation. It is estimated to host up to 10(26) microbial cells that may intercept part of the photon flux impinging on the leaves. Based on 454-pyrosequencing-generated metagenome data, we report on the existence of diverse microbial rhodopsins in five distinct phyllospheres from tamarisk (Tamarix nilotica), soybean (Glycine max), Arabidopsis (Arabidopsis thaliana), clover (Trifolium repens) and rice (Oryza sativa). Our findings, for the first time describing microbial rhodopsins from non-aquatic habitats, point towards the potential coexistence of microbial rhodopsin-based phototrophy and plant chlorophyll-based photosynthesis, with the different pigments absorbing non-overlapping fractions of the light spectrum.

MeSH Terms
Ecosystem Light Metagenome Photosynthesis Phototrophic Processes Phylogeny Plant Leaves/microbiology Plants/microbiology Rhodopsins, Microbial/analysis
Chemicals
Rhodopsins, Microbial
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Atamna-Ismaeel Nof
Faculty of Biology, Lorry I Lokey Interdisciplinary Center for Life Sciences and Engineering, Faculty of Computer Science, Technion - Israel Institute of Technology, Haifa 32000, Israel.
Finkel Omri M
Glaser Fabian
Sharon Itai
Schneider Ron
Post Anton F
Spudich John L
von Mering Christian
Vorholt Julia A
Iluz David
Béjà Oded
Belkin Shimshon
References (37)
37 references, click to expand
  1. Light stimulates growth of proteorhodopsin-containing marine Flavobacteria.
    Nature. 2007 Jan 11;445(7124):210-3 PMID: 17215843
  2. Proteorhodopsin in the ubiquitous marine bacterium SAR11.
    Nature. 2005 Nov 3;438(7064):82-5 PMID: 16267553
  3. Microbiology of the phyllosphere.
    Appl Environ Microbiol. 2003 Apr;69(4):1875-83 PMID: 12676659
  4. Upcoming challenges for multiple sequence alignment methods in the high-throughput era.
    Bioinformatics. 2009 Oct 1;25(19):2455-65 PMID: 19648142
  5. Proteorhodopsin-bearing bacteria in Antarctic sea ice.
    Appl Environ Microbiol. 2010 Sep;76(17):5918-25 PMID: 20601510
  6. Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria.
    ISME J. 2009 Jun;3(6):726-37 PMID: 19242530
  7. AQUA: automated quality improvement for multiple sequence alignments.
    Bioinformatics. 2010 Jan 15;26(2):263-5 PMID: 19926669
  8. Estimating maximum likelihood phylogenies with PhyML.
    Methods Mol Biol. 2009;537:113-37 PMID: 19378142
  9. Xanthorhodopsin: a bacteriorhodopsin-like proton pump with a carotenoid antenna.
    Biochim Biophys Acta. 2008 Jul-Aug;1777(7-8):684-8 PMID: 18515067
  10. Adaptation and spectral tuning in divergent marine proteorhodopsins from the eastern Mediterranean and the Sargasso Seas.
    ISME J. 2007 May;1(1):48-55 PMID: 18043613
  11. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific.
    PLoS Biol. 2007 Mar;5(3):e77 PMID: 17355176
  12. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria.
    Proc Natl Acad Sci U S A. 2009 Sep 22;106(38):16428-33 PMID: 19805315
  13. Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation.
    PLoS Biol. 2010 Apr 27;8(4):e1000358 PMID: 20436956
  14. The multitalented microbial sensory rhodopsins.
    Trends Microbiol. 2006 Nov;14(11):480-7 PMID: 17005405
  15. Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea.
    Nature. 2006 Feb 16;439(7078):847-50 PMID: 16482157
  16. Quantitative metagenomic analyses based on average genome size normalization.
    Appl Environ Microbiol. 2011 Apr;77(7):2513-21 PMID: 21317268
  17. Diversification and spectral tuning in marine proteorhodopsins.
    EMBO J. 2003 Apr 15;22(8):1725-31 PMID: 12682005
  18. Rhodopsin-like protein from the purple membrane of Halobacterium halobium.
    Nat New Biol. 1971 Sep 29;233(39):149-52 PMID: 4940442
  19. Drop-size soda lakes: transient microbial habitats on a salt-secreting desert tree.
    Genetics. 2008 Mar;178(3):1615-22 PMID: 18245835
  20. Plant-associated methylobacteria as co-evolved phytosymbionts: a hypothesis.
    Plant Signal Behav. 2007 Mar;2(2):74-8 PMID: 19516971
  21. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes.
    BMC Bioinformatics. 2008 Sep 19;9:386 PMID: 18803844
  22. Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna.
    Science. 2005 Sep 23;309(5743):2061-4 PMID: 16179480
  23. Dendroscope: An interactive viewer for large phylogenetic trees.
    BMC Bioinformatics. 2007 Nov 22;8:460 PMID: 18034891
  24. Green light: a signal to slow down or stop.
    J Exp Bot. 2007;58(12):3099-111 PMID: 17630292
  25. Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies.
    Science. 1990 Jan 19;247(4940):329-32 PMID: 17735851
  26. Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems.
    ISME J. 2008 Jun;2(6):656-62 PMID: 18369329
  27. Primary production of the biosphere: integrating terrestrial and oceanic components
    Science. 1998 Jul 10;281(5374):237-40 PMID: 9657713
  28. Actinorhodopsins: proteorhodopsin-like gene sequences found predominantly in non-marine environments.
    Environ Microbiol. 2008 Apr;10(4):1039-56 PMID: 18218036
  29. New insights into metabolic properties of marine bacteria encoding proteorhodopsins.
    PLoS Biol. 2005 Aug;3(8):e273 PMID: 16008504
  30. Assessing diversity and biogeography of aerobic anoxygenic phototrophic bacteria in surface waters of the Atlantic and Pacific Oceans using the Global Ocean Sampling expedition metagenomes.
    Environ Microbiol. 2007 Jun;9(6):1464-75 PMID: 17504484
  31. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea.
    Science. 2000 Sep 15;289(5486):1902-6 PMID: 10988064
  32. Abundant and diverse bacteria involved in DMSP degradation in marine surface waters.
    Environ Microbiol. 2008 Sep;10(9):2397-410 PMID: 18510552
  33. Proteorhodopsin genes are distributed among divergent marine bacterial taxa.
    Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12830-5 PMID: 14566056
  34. Complete genome sequence of "Candidatus Puniceispirillum marinum" IMCC1322, a representative of the SAR116 clade in the Alphaproteobacteria.
    J Bacteriol. 2010 Jun;192(12):3240-1 PMID: 20382761
  35. Bacterial colonization of leaves: a spectrum of strategies.
    Phytopathology. 1999 May;89(5):353-9 PMID: 18944746
  36. Proteorhodopsin phototrophy in the ocean.
    Nature. 2001 Jun 14;411(6839):786-9 PMID: 11459054
  37. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix.
    Mol Biol Evol. 2009 Jul;26(7):1641-50 PMID: 19377059
Article Info
Journal
Environmental microbiology
Abbr.
Environ Microbiol
ISSN
1462-2920
Published
2012-01-00
Epub
2011-00-01
Pages
140-6
Language
English
Region
England
NLM ID
100883692
PMCID
PMC3608849
Subset
IM
Grants
NIGMS NIH HHS · R37 GM027750 · United States
NIGMS NIH HHS · R37GM27750 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com