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Orphan Hybrid Histidine Protein Kinase SinK Acts as a Signal Integrator To Fine-Tune Multicellular Behavior in Myxococcus xanthus

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Glaser,  Maike
Department of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Higgs,  Penelope I.
Department of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Citation

Glaser, M., & Higgs, P. I. (2019). Orphan Hybrid Histidine Protein Kinase SinK Acts as a Signal Integrator To Fine-Tune Multicellular Behavior in Myxococcus xanthus. JOURNAL OF BACTERIOLOGY, 201(6): e00561. doi:10.1128/JB.00561-18.


Cite as: https://hdl.handle.net/21.11116/0000-0008-BF44-5
Abstract
His-Asp phosphorelay (also known as two-component signal transduction)
proteins are the predominant mechanism used in most bacteria to control
behavior in response to changing environmental conditions. In addition
to systems consisting of a simple two-component system utilizing an
isolated histidine kinase/response regulator pair, some bacteria are
enriched in histidine kinases that serve as signal integration proteins;
these kinases are usually characterized by noncanonical domain
architecture, and the responses that they regulate may be difficult to
identify. The environmental bacterium Myxococcus xanthus is highly
enriched in these noncanonical histidine kinases. M. xanthus is renowned
for a starvation-induced multicellular developmental program in which
some cells are induced to aggregate into fruiting bodies and then
differentiate into environmentally resistant spores. Here, we
characterize the M. xonthus orphan hybrid histidine kinase SinK
(Mxan_4465), which consists of a histidine kinase transmitter followed
by two receiver domains (REC1 and REC2). Nonphosphorylatable sinK
mutants were analyzed under two distinct developmental conditions and
using a new high-resolution developmental assay. These assays revealed
that SinK autophosphorylation and REC1 impact the onset of aggregation
and/or the mobility of aggregates, while REC2 impacts sporulation
efficiency. SinK activity is controlled by a genus-specific hypothetical
protein (SinM; Mxan_4466). We propose that SinK serves to fine-tune
fruiting body morphology in response to environmental conditions.
IMPORTANCE Biofilms are multicellular communities of microorganisms that
play important roles in host disease or environmental biofouling. Design
of preventative strategies to block biofilms depends on understanding
the molecular mechanisms used by microorganisms to build them. The
production of biofilms in bacteria often involves two-component signal
transduction systems in which one protein component (a kinase) detects
an environmental signal and, through phosphotransfer, activates a second
protein component (a response regulator) to change the transcription of
genes necessary to produce a biofilm. We show that an atypical kinase,
Sink, modulates several distinct stages of specialized biofilm produced
by the environmental bacterium Myxococcus xonthus. Sink likely
integrates multiple signals to fine-tune biofilm formation in response
to distinct environmental conditions.