Unique function of the bacterial chromosome segregation machinery in apically growing streptomyces - targeting the chromosome to new hyphal tubes and its anchorage at the tips

Agnieszka Kois-Ostrowska, Agnieszka Strzałka, Natalia Lipietta, Emma Tilley, Jolanta Zakrzewska-Czerwińska, Paul Herron, Dagmara Jakimowicz

Research output: Contribution to journalArticle

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Abstract

The coordination of chromosome segregation with cell growth is fundamental to the proliferation of any organism. In most unicellular bacteria, chromosome segregation is strictly coordinated with cell division and involves ParA that moves the ParB nucleoprotein complexes bi- or unidirectionally toward the cell pole(s). However, the chromosome organization in multiploid, apically extending and branching Streptomyces hyphae challenges the known mechanisms of bacterial chromosome segregation. The complex Streptomyces life cycle involves two stages: vegetative growth and sporulation. In the latter stage, multiple cell divisions accompanied by chromosome compaction and ParAB assisted segregation turn multigenomic hyphal cell into a chain of unigenomic spores. However, the requirement for active chromosome segregation is unclear in the absence of canonical cell division during vegetative growth except in the process of branch formation. The mechanism by which chromosomes are targeted to new hyphae in streptomycete vegetative growth has remained unknown until now. Here, we address the question of whether active chromosome segregation occurs at this stage. Applied for the first time in Streptomyces, labelling of the chromosomal replication initiation region (oriC) and time-lapse microscopy, revealed that in vegetative hyphae every copy of the chromosome is complexed with ParB, whereas ParA, through interaction with the apical protein complex (polarisome), tightly anchors only one chromosome at the hyphal tip. The anchor is maintained during replication, when ParA captures one of the daughter oriCs. During spore germination and branching, ParA targets one of the multiple chromosomal copies to the new hyphal tip, enabling efficient elongation of hyphal tube. Thus, our studies reveal a novel role for ParAB proteins during hyphal tip establishment and extension.

Original languageEnglish
Article numbere1006488
Number of pages25
JournalPLOS Genetics
Volume12
Issue number12
DOIs
Publication statusPublished - 15 Dec 2016

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Bacterial Chromosomes
Chromosome Segregation
chromosome segregation
Streptomyces
machinery
targeting
chromosome
Chromosomes
Hyphae
chromosomes
Cell Division
hyphae
vegetative growth
cell division
Growth
Spores
branching
nucleoproteins
Nucleoproteins
spore germination

Keywords

  • chromosome segregation
  • cell growth
  • Streptomyces
  • ParAB proteins
  • g hyphal tip establishment
  • h chromosomal anchorage
  • chromosome targeting
  • unicellular bacteria

Cite this

Kois-Ostrowska, Agnieszka ; Strzałka, Agnieszka ; Lipietta, Natalia ; Tilley, Emma ; Zakrzewska-Czerwińska, Jolanta ; Herron, Paul ; Jakimowicz, Dagmara. / Unique function of the bacterial chromosome segregation machinery in apically growing streptomyces - targeting the chromosome to new hyphal tubes and its anchorage at the tips. In: PLOS Genetics. 2016 ; Vol. 12, No. 12.
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Unique function of the bacterial chromosome segregation machinery in apically growing streptomyces - targeting the chromosome to new hyphal tubes and its anchorage at the tips. / Kois-Ostrowska, Agnieszka; Strzałka, Agnieszka; Lipietta, Natalia; Tilley, Emma; Zakrzewska-Czerwińska, Jolanta; Herron, Paul; Jakimowicz, Dagmara.

In: PLOS Genetics, Vol. 12, No. 12, e1006488, 15.12.2016.

Research output: Contribution to journalArticle

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AU - Kois-Ostrowska, Agnieszka

AU - Strzałka, Agnieszka

AU - Lipietta, Natalia

AU - Tilley, Emma

AU - Zakrzewska-Czerwińska, Jolanta

AU - Herron, Paul

AU - Jakimowicz, Dagmara

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AB - The coordination of chromosome segregation with cell growth is fundamental to the proliferation of any organism. In most unicellular bacteria, chromosome segregation is strictly coordinated with cell division and involves ParA that moves the ParB nucleoprotein complexes bi- or unidirectionally toward the cell pole(s). However, the chromosome organization in multiploid, apically extending and branching Streptomyces hyphae challenges the known mechanisms of bacterial chromosome segregation. The complex Streptomyces life cycle involves two stages: vegetative growth and sporulation. In the latter stage, multiple cell divisions accompanied by chromosome compaction and ParAB assisted segregation turn multigenomic hyphal cell into a chain of unigenomic spores. However, the requirement for active chromosome segregation is unclear in the absence of canonical cell division during vegetative growth except in the process of branch formation. The mechanism by which chromosomes are targeted to new hyphae in streptomycete vegetative growth has remained unknown until now. Here, we address the question of whether active chromosome segregation occurs at this stage. Applied for the first time in Streptomyces, labelling of the chromosomal replication initiation region (oriC) and time-lapse microscopy, revealed that in vegetative hyphae every copy of the chromosome is complexed with ParB, whereas ParA, through interaction with the apical protein complex (polarisome), tightly anchors only one chromosome at the hyphal tip. The anchor is maintained during replication, when ParA captures one of the daughter oriCs. During spore germination and branching, ParA targets one of the multiple chromosomal copies to the new hyphal tip, enabling efficient elongation of hyphal tube. Thus, our studies reveal a novel role for ParAB proteins during hyphal tip establishment and extension.

KW - chromosome segregation

KW - cell growth

KW - Streptomyces

KW - ParAB proteins

KW - g hyphal tip establishment

KW - h chromosomal anchorage

KW - chromosome targeting

KW - unicellular bacteria

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DO - 10.1371/journal.pgen.1006488

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