Literature DB >> 26055115

ABC Transporter Required for Intercellular Transfer of Developmental Signals in a Heterocystous Cyanobacterium.

Patrick Videau1, Orion S Rivers1, Kelly C Higa1, Sean M Callahan2.   

Abstract

UNLABELLED: In the filamentous cyanobacterium Anabaena, patS and hetN encode peptide-derived signals with many of the properties of morphogens. These signals regulate the formation of a periodic pattern of heterocysts by lateral inhibition of differentiation. Here we show that intercellular transfer of the patS- and hetN-dependent developmental signals from heterocysts to vegetative cells requires HetC, a predicted ATP-binding cassette transporter (ABC transporter). Relative to the wild type, in a hetC mutant differentiation resulted in a reduced number of heterocysts that were incapable of nitrogen fixation, but deletion of patS or hetN restored heterocyst number and function in a hetC background. These epistasis results suggest that HetC is necessary for conferring self-immunity to the inhibitors on differentiating cells. Nine hours after induction of differentiation, HetC was required for neither induction of transcription of patS nor intercellular transfer of the patS-encoded signal to neighboring cells. Conversely, in strains lacking HetC, the patS- and hetN-encoded signals were not transferred from heterocyst cells to adjacent vegetative cells. The results support a model in which the patS-dependent signal is initially transferred between vegetative cells in a HetC-independent fashion, but some time before morphological differentiation of heterocysts is complete, transfer of both signals transitions to a HetC-dependent process. IMPORTANCE: How chemical cues that regulate pattern formation in multicellular organisms move from one cell to another is a central question in developmental biology. In this study, we show that an ABC transporter, HetC, is necessary for transport of two developmental signals between different types of cells in a filamentous cyanobacterium. ABC transporters are found in organisms as diverse as bacteria and humans and, as the name implies, are often involved in the transport of molecules across a cellular membrane. The activity of HetC was shown to be required for signaling between heterocysts, which supply fixed nitrogen to the organism, and other cells, as well as for conferring immunity to self-signaling on developing heterocysts.
Copyright © 2015, American Society for Microbiology. All Rights Reserved.

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Year:  2015        PMID: 26055115      PMCID: PMC4507337          DOI: 10.1128/JB.00304-15

Source DB:  PubMed          Journal:  J Bacteriol        ISSN: 0021-9193            Impact factor:   3.490


  44 in total

1.  Inactivation of patS and hetN causes lethal levels of heterocyst differentiation in the filamentous cyanobacterium Anabaena sp. PCC 7120.

Authors:  Pritty B Borthakur; Christine C Orozco; Shirley S Young-Robbins; Robert Haselkorn; Sean M Callahan
Journal:  Mol Microbiol       Date:  2005-07       Impact factor: 3.501

2.  Regulation by hetC of genes required for heterocyst differentiation and cell division in Anabaena sp. strain PCC 7120.

Authors:  Yu Wang; Xudong Xu
Journal:  J Bacteriol       Date:  2005-12       Impact factor: 3.490

3.  Is the periplasm continuous in filamentous multicellular cyanobacteria?

Authors:  Enrique Flores; Antonia Herrero; C Peter Wolk; Iris Maldener
Journal:  Trends Microbiol       Date:  2006-08-23       Impact factor: 17.079

Review 4.  Models of biological pattern formation: from elementary steps to the organization of embryonic axes.

Authors:  Hans Meinhardt
Journal:  Curr Top Dev Biol       Date:  2008       Impact factor: 4.897

5.  Epistasis analysis of four genes from Anabaena sp. strain PCC 7120 suggests a connection between PatA and PatS in heterocyst pattern formation.

Authors:  Christine C Orozco; Douglas D Risser; Sean M Callahan
Journal:  J Bacteriol       Date:  2006-03       Impact factor: 3.490

6.  Heterocyst pattern formation controlled by a diffusible peptide.

Authors:  H S Yoon; J W Golden
Journal:  Science       Date:  1998-10-30       Impact factor: 47.728

7.  Suppression of heterocyst differentiation in Anabaena PCC 7120 by a cosmid carrying wild-type genes encoding enzymes for fatty acid synthesis.

Authors:  C C Bauer; K S Ramaswamy; S Endley; L A Scappino; J W Golden; R Haselkorn
Journal:  FEMS Microbiol Lett       Date:  1997-06-01       Impact factor: 2.742

8.  hetC, a gene coding for a protein similar to bacterial ABC protein exporters, is involved in early regulation of heterocyst differentiation in Anabaena sp. strain PCC 7120.

Authors:  I Khudyakov; C P Wolk
Journal:  J Bacteriol       Date:  1997-11       Impact factor: 3.490

9.  Multidrug resistance-associated protein MRP-1 regulates dauer diapause by its export activity in Caenorhabditis elegans.

Authors:  Tomoko Yabe; Norio Suzuki; Tatsuhiko Furukawa; Takeshi Ishihara; Isao Katsura
Journal:  Development       Date:  2005-07       Impact factor: 6.868

Review 10.  Structure, function, and evolution of bacterial ATP-binding cassette systems.

Authors:  Amy L Davidson; Elie Dassa; Cedric Orelle; Jue Chen
Journal:  Microbiol Mol Biol Rev       Date:  2008-06       Impact factor: 11.056

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  9 in total

1.  The heterocyst regulatory protein HetP and its homologs modulate heterocyst commitment in Anabaena sp. strain PCC 7120.

Authors:  Patrick Videau; Orion S Rivers; Kathryn Hurd; Blake Ushijima; Reid T Oshiro; Rachel J Ende; Samantha M O'Hanlon; Loralyn M Cozy
Journal:  Proc Natl Acad Sci U S A       Date:  2016-10-24       Impact factor: 11.205

2.  Three Substrains of the Cyanobacterium Anabaena sp. Strain PCC 7120 Display Divergence in Genomic Sequences and hetC Function.

Authors:  Yali Wang; Yuan Gao; Chao Li; Hong Gao; Cheng-Cai Zhang; Xudong Xu
Journal:  J Bacteriol       Date:  2018-06-11       Impact factor: 3.490

3.  Phenotypic Assessment Suggests Multiple Start Codons for HetN, an Inhibitor of Heterocyst Differentiation, in Anabaena sp. Strain PCC 7120.

Authors:  Orion S Rivers; Silvia Beurmann; Allexa Dow; Loralyn M Cozy; Patrick Videau
Journal:  J Bacteriol       Date:  2018-07-25       Impact factor: 3.490

4.  Interaction network among factors involved in heterocyst-patterning in cyanobacteria.

Authors:  Xiaomei Xu; Raphaël Rachedi; Maryline Foglino; Emmanuel Talla; Amel Latifi
Journal:  Mol Genet Genomics       Date:  2022-05-17       Impact factor: 3.291

5.  Mutation of the murC and murB Genes Impairs Heterocyst Differentiation in Anabaena sp. Strain PCC 7120.

Authors:  Patrick Videau; Orion S Rivers; Blake Ushijima; Reid T Oshiro; Min Joo Kim; Benjamin Philmus; Loralyn M Cozy
Journal:  J Bacteriol       Date:  2016-03-31       Impact factor: 3.490

6.  Terminal heterocyst differentiation in the Anabaena patA mutant as a result of post-transcriptional modifications and molecular leakage.

Authors:  Pau Casanova-Ferrer; Saúl Ares; Javier Muñoz-García
Journal:  PLoS Comput Biol       Date:  2022-08-15       Impact factor: 4.779

7.  Robust stochastic Turing patterns in the development of a one-dimensional cyanobacterial organism.

Authors:  Francesca Di Patti; Laura Lavacchi; Rinat Arbel-Goren; Leora Schein-Lubomirsky; Duccio Fanelli; Joel Stavans
Journal:  PLoS Biol       Date:  2018-05-04       Impact factor: 8.029

8.  The Ser/Thr Kinase PknH Is Essential for Maintaining Heterocyst Pattern in the Cyanobacterium Anabaena sp. Strain PCC 7120.

Authors:  Shun-Ichi Fukushima; Shigeki Ehira
Journal:  Life (Basel)       Date:  2018-08-24

9.  The First Proteomics Study of Nostoc sp. PCC 7120 Exposed to Cyanotoxin BMAA under Nitrogen Starvation.

Authors:  Olga A Koksharova; Ivan O Butenko; Olga V Pobeguts; Nina A Safronova; Vadim M Govorun
Journal:  Toxins (Basel)       Date:  2020-05-09       Impact factor: 4.546

  9 in total

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