Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2015 Sep 14;198(3):377-85.
doi: 10.1128/JB.00474-15. Print 2016 Feb 1.

Two-Component Signal Transduction Systems That Regulate the Temporal and Spatial Expression of Myxococcus xanthus Sporulation Genes

Zaara Sarwar  1 , Anthony G Garza  2
Affiliations
Review

Two-Component Signal Transduction Systems That Regulate the Temporal and Spatial Expression of Myxococcus xanthus Sporulation Genes

Zaara Sarwar et al. J Bacteriol. .

Abstract

When starved for nutrients, Myxococcus xanthus produces a biofilm that contains a mat of rod-shaped cells, known as peripheral rods, and aerial structures called fruiting bodies, which house thousands of dormant and stress-resistant spherical spores. Because rod-shaped cells differentiate into spherical, stress-resistant spores and spore differentiation occurs only in nascent fruiting bodies, many genes and multiple levels of regulation are required. Over the past 2 decades, many regulators of the temporal and spatial expression of M. xanthus sporulation genes have been uncovered. Of these sporulation gene regulators, two-component signal transduction circuits, which typically contain a histidine kinase sensor protein and a transcriptional regulator known as response regulator, are among the best characterized. In this review, we discuss prototypical two-component systems (Nla6S/Nla6 and Nla28S/Nla28) that regulate an early, preaggregation phase of sporulation gene expression during fruiting body development. We also discuss orphan response regulators (ActB and FruA) that regulate a later phase of sporulation gene expression, which begins during the aggregation stage of fruiting body development. In addition, we summarize the research on a complex two-component system (Esp) that is important for the spatial regulation of sporulation.

PubMed Disclaimer

Figures

FIG 1
FIG 1
The Myxococcus xanthus life cycle. M. xanthus is a microbial predator that obtains nutrients by forming swarming biofilms and collectively feeding on other bacteria. When prey bacteria are not available to provide nutrients, cells undergo a multicellular developmental cycle that culminates with the formation of spore-filled fruiting bodies. The stages of development include preaggregation (1 to 5 h poststarvation), aggregation and mound formation (6 to 18 h poststarvation), and sporulation (24 to 120 h poststarvation). Sporulation occurs inside the dome-shaped mounds and is the process by which rod-shaped cells are converted into spherical, stress-resistant spores. The availability of nutrients, which presumably are provided by prey bacteria, triggers spore germination and, eventually, the formation of swarms that engage in group feeding.
FIG 2
FIG 2
Diagram of the Nla6S/Nla6 and Nla28S/Nla28 two-component systems. Nla6S/Nla6 and Nla28S/Nla28 are early-acting two-component systems that directly regulate expression of sporulation genes. Nla6S and Nla28S are predicted to be cytoplasmic and membrane-bound histidine kinase sensors, respectively (28). The signal detected by Nla6S is unknown; however, it has been proposed that the cell density reporter known as A-signal or nutrient levels (starvation) may be the activating signal for Nla28S (67). It is believed that Nla6S modulates the activity of the Nla6 response regulator via dephosphorylation, whereas Nla28S modulates the activity of the Nla28 response regulator via phosphorylation (38, 67). Nla6 is a transcriptional activator that regulates genetic loci such as exo, MXAN2688, and MXAN3259 that are important for spore differentiation and spore stress resistance (59). Nla28 is a transcriptional activator that regulates genetic loci such as cusBA and MXAN7147, which are primarily involved in spore stress resistance (Li et al., unpublished). Nla6 and Nla28 also modulate expression of other transcriptional regulators that are important for sporulation: Nla6 modulates expression of actB and nla28, and Nla28 modulates expression of actB, mrpAB, and nla6 (43) (Li et al., unpublished). In addition, Nla6 and Nla28 are involved in autoregulation (43).
FIG 3
FIG 3
Expression of an actB::lacZ fusion in fruiting body cells and peripheral rods. Cells were harvested at 24 h of development, and the fruiting body cells and peripheral rods were separated by differential centrifugation as previously described (98). Mean β-galactosidase-specific activities from three independent replicates are shown (Garza, unpublished). Error bars are standard deviations of the means.
FIG 4
FIG 4
Diagram of the Esp two-component pathway. Esp is a complex two-component pathway that regulates the timing of sporulation (92, 93, 95). This two-component pathway consists of the following proteins: the cytoplasmic EspA and membrane-bound EspC hybrid histidine kinases, which contain a histidine kinase transmitter domain and a response regulator receiver domain, the serine/threonine protein kinases called PktA5 and PktB8, and the putative EspB oligopeptide transport membrane protein. Several lines of evidence indicate that EspA and EspC form a signaling unit; EspA performs autophosphorylation via its transmitter domain and then transfers a phosphoryl group to its receiver domain and the receiver domain of EspC (94). It has been proposed that EspB, PktA5, and PktB8 work together to modulate the activity of EspA (92, 95). It is believed that the EspAC signaling unit directly or indirectly inhibits the accumulation of MrpC, which is a positive regulator of sporulation, until the proper time in fruiting body development (97). SD, sensor domain; DHp, dimerization and histidine phosphorylation domain; CA, catalytic and ATP binding domain; REC, receiver domain.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Dickschat JS, Wenzel SC, Bode HB, Muller R, Schulz S. 2004. Biosynthesis of volatiles by the myxobacterium Myxococcus xanthus. Chembiochem 5:778–787. doi:10.1002/cbic.200300813. - DOI - PubMed
    1. Berleman JE, Kirby JR. 2009. Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol Rev 33:942–957. doi:10.1111/j.1574-6976.2009.00185.x. - DOI - PMC - PubMed
    1. Rosenberg E, Keller KH, Dworkin M. 1977. Cell density-dependent growth of Myxococcus xanthus on casein. J Bacteriol 129:770–777. - PMC - PubMed
    1. Varon M, Cohen S, Rosenberg E. 1984. Autocides produced by Myxococcus xanthus. J Bacteriol 160:1146–1150. - PMC - PubMed
    1. O'Connor KA, Zusman DR. 1991. Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J Bacteriol 173:3318–3333. - PMC - PubMed

Publication types

MeSH terms

LinkOut - more resources