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<meta name="description" content="Certain mutations in the dev CRISPR-Cas (clustered regularly interspaced short palindromic repeat-associated) system of Myxococcus xanthus impair sporulation. The link between development and a CRISPR-Cas system has been a mystery. Surprisingly, DNA sequencing of natural isolates revealed that many …"><meta name="keywords" content="pmid:25645563, PMC4352663, doi:10.1128/JB.02542-14, Research Support, Non-U.S. Gov&#x27;t, Research Support, U.S. Gov&#x27;t, Non-P.H.S., Ramya Rajagopalan, Sébastien Wielgoss, Lee Kroos, Bacterial Proteins / genetics, Bacterial Proteins / metabolism*, Codon, Terminator, DNA, Bacterial, Evolution, Molecular, Gene Expression Regulation, Bacterial / physiology*, Mutation, Myxococcus xanthus / genetics, Myxococcus xanthus / growth &amp; development, Myxococcus xanthus / metabolism*, Operon, Spores, Bacterial / physiology, PubMed Abstract, NIH, NLM, NCBI, National Institutes of Health, National Center for Biotechnology Information, National Library of Medicine, MEDLINE"><meta name="robots" content="index,nofollow,noarchive"><meta property="og:title" content="devI is an evolutionarily young negative regulator of Myxococcus xanthus development - PubMed"><meta property="og:url" content="https://pubmed.ncbi.nlm.nih.gov/25645563/"><meta property="og:description" content="Certain mutations in the dev CRISPR-Cas (clustered regularly interspaced short palindromic repeat-associated) system of Myxococcus xanthus impair sporulation. The link between development and a CRISPR-Cas system has been a mystery. Surprisingly, DNA sequencing of natural isolates revealed that many …"><meta property="og:image" content="https://cdn.ncbi.nlm.nih.gov/pubmed/persistent/pubmed-meta-image-v2.jpg"><meta property="og:image:secure_url" content="https://cdn.ncbi.nlm.nih.gov/pubmed/persistent/pubmed-meta-image-v2.jpg"><meta property="og:type" content="website"><meta property="og:site_name" content="PubMed"><meta name="twitter:domain" content="pubmed.ncbi.nlm.nih.gov"><meta name="twitter:card" content="summary_large_image"><meta name="twitter:title" content="devI is an evolutionarily young negative regulator of Myxococcus xanthus development - PubMed"><meta name="twitter:url" content="https://pubmed.ncbi.nlm.nih.gov/25645563/"><meta name="twitter:description" content="Certain mutations in the dev CRISPR-Cas (clustered regularly interspaced short palindromic repeat-associated) system of Myxococcus xanthus impair sporulation. The link between development and a CRISPR-Cas system has been a mystery. Surprisingly, DNA sequencing of natural isolates revealed that many …"><meta name="twitter:image" content="https://cdn.ncbi.nlm.nih.gov/pubmed/persistent/pubmed-meta-image-v2.jpg">
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<input type="email" aria-label="Sender Email Address" placeholder="email@example.com" id="email-from" class="email-from" pattern="^[a-zA-Z0-9_.+-]+@[a-zA-Z0-9-]+\.[a-zA-Z0-9-.]+$" maxlength="256">
</div>
<div class="action-panel-control-wrap">
<label for="email-citation-format" class="action-panel-label">
Format:
</label>
<select id="email-citation-format" name="citation-format" class="action-panel-selector email-citation-format">
<option selected="selected" value="summary">Summary</option>
<option value="summary-text">Summary (text)</option>
<option value="abstract">Abstract</option>
<option value="abstract-text">Abstract (text)</option>
</select>
</div>
<div class="include-supplemental-container">
<input type="checkbox" aria-label="Include MeSH and other data" name="include-supplemental" id="email-include-supplemental" class="email-include-supplemental">
<label for="email-include-supplemental" class="email-include-supplemental-label">MeSH and other data</label>
</div>
<div class="form-field recaptcha ">
<div class="g-recaptcha" id="id-recaptcha" data-sitekey="6LfsWHMdAAAAAClKbtOpjQ2pMjgsGxvv7NdZW9uI"></div>
</div>
<div id="captcha-error-message" class="usa-input-error-message captcha-validation-message" role="alert"></div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Sending..."
data-ga-category="save_share"
data-ga-action="email"
data-ga-label="send">
Send email
</button>
<button class="action-panel-cancel"
aria-label="Close 'Email citations' panel"
ref="linksrc=close_email_panel"
aria-controls="email-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="email"
data-ga-label="cancel">
Cancel
</button>
</div>
<input type="hidden" name="email-search-details" value="" />
<input type="hidden" name="email-search-details-hash" value="0e42663a6c3bd85498fcb88798998fed7bfdc45d457db35281e41afe13cc0524" />
</form>
</div>
</div>
<div id="collections-action-panel"
class="collections-action-panel action-panel in-progress-dots-panel"
aria-hidden="true"
data-collections-open-panel-enabled="false"
data-collections-open-panel-url-hash="#open-collections-panel">
<div class="inner-wrap">
<h3 class="action-panel-heading">
Add to Collections
</h3>
<form id="collections-action-panel-form"
class="collections-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
data-existing-collections-url="/list-existing-collections/"
data-add-to-existing-collection-url="/add-to-existing-collection/"
data-create-and-add-to-new-collection-url="/create-and-add-to-new-collection/"
data-get-article-ids-by-search-url="/get-article-ids-by-search/"
data-myncbi-max-collection-name-length="100"
data-add-to-collection-max-amount="1000"
data-collections-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/">
<input type="hidden" name="csrfmiddlewaretoken" value="Wvagi4pBKNgbPkim3itZiwMhtAW4U3ISdiUlVUSXko3FJLocGB61MEiV1EEgNEgc">
<div class="choice-group" role="radiogroup">
<ul class="radio-group-items">
<li>
<input type="radio"
id="collections-action-panel-new"
class="collections-new"
name="collections"
value="new"
data-ga-category="save_share"
data-ga-action="collections"
data-ga-label="collections_radio_new">
<label for="collections-action-panel-new">Create a new collection</label>
</li>
<li>
<input type="radio"
id="collections-action-panel-existing"
class="collections-existing"
name="collections"
value="existing"
checked="true"
data-ga-category="save_share"
data-ga-action="collections"
data-ga-label="collections_radio_existing">
<label for="collections-action-panel-existing">Add to an existing collection</label>
</li>
</ul>
</div>
<div class="controls-wrapper">
<div class="action-panel-control-wrap new-collections-controls">
<label for="collections-action-panel-add-to-new" class="action-panel-label required-field-asterisk">
Name your collection:
</label>
<input
type="text"
name="add-to-new-collection"
id="collections-action-panel-add-to-new"
class="collections-action-add-to-new"
pattern="[^&quot;&amp;=&lt;&gt;\/]*" title="The following characters are not allowed in the Name field: &quot;&amp;=&lt;&gt;/"
maxlength="100"
data-ga-category="save_share"
data-ga-action="create_collection"
data-ga-label="non_favorties_collection">
<div class="collections-new-name-too-long usa-input-error-message selection-validation-message">
Name must be less than 100 characters
</div>
</div>
<div class="action-panel-control-wrap existing-collections-controls">
<label for="collections-action-panel-add-to-existing" class="action-panel-label">
Choose a collection:
</label>
<select id="collections-action-panel-add-to-existing"
class="action-panel-selector collections-action-add-to-existing"
data-ga-category="save_share"
data-ga-action="select_collection"
data-ga-label="($('#collections-action-add-to-existing').val() === 'Favorites') ? 'Favorites' : 'non_favorites_collection'">
</select>
<div class="collections-retry-load-on-error usa-input-error-message selection-validation-message">
Unable to load your collection due to an error<br>
<a href="#">Please try again</a>
</div>
</div>
</div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Adding..."
data-pinger-ignore
data-ga-category="save_share"
data-ga-action="collections"
data-ga-label="add">
Add
</button>
<button class="action-panel-cancel"
aria-label="Close 'Add to Collections' panel"
ref="linksrc=close_collections_panel"
aria-controls="collections-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="collections"
data-ga-label="cancel">
Cancel
</button>
</div>
</form>
</div>
</div>
<div id="bibliography-action-panel"
class="bibliography-action-panel action-panel in-progress-dots-panel"
aria-hidden="true"
data-bibliography-open-panel-enabled="false"
data-bibliography-open-panel-url-hash="#open-bibliography-panel">
<div class="inner-wrap">
<h3 class="action-panel-heading">
Add to My Bibliography
</h3>
<form id="bibliography-action-panel-form"
class="bibliography-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
data-add-to-bibliography-max-amount="100"
data-add-to-bibliography-batch-size="10"
data-bibliography-delegates-url="/list-bibliography-delegates/"
data-add-to-bibliography-url="/add-to-bibliography/"
data-get-article-ids-by-search-url="/get-article-ids-by-search/"
data-mybib-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/mybibliography/">
<input type="hidden" name="csrfmiddlewaretoken" value="Wvagi4pBKNgbPkim3itZiwMhtAW4U3ISdiUlVUSXko3FJLocGB61MEiV1EEgNEgc">
<div class="action-panel-control-wrap bibliographies-controls">
<div class="choice-group">
<ul class="bibliographies-action-add radio-group-items">
<li>
<input name="bibliography" id="my-bibliography" class="my-bibliography" type="radio" checked/>
<label for="my-bibliography">My Bibliography</label>
</li>
</ul>
</div>
</div>
<div class="bibliographies-retry-load-on-error usa-input-error-message selection-validation-message">
Unable to load your delegates due to an error<br>
<a href="#">Please try again</a>
</div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Adding..."
data-pinger-ignore>
Add
</button>
<button class="action-panel-cancel"
aria-label="Close 'Add to bibliography' panel"
ref="linksrc=close_bibliography_panel"
aria-controls="bibliography-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="mybib"
data-ga-label="cancel">
Cancel
</button>
</div>
</form>
</div>
</div>
<div id="saved-search-action-panel" class="saved-search-action-panel action-panel " aria-hidden="true"
data-saved-search-open-panel-enabled="false"
data-saved-search-open-panel-url-hash="#open-saved-search-panel">
<div class="inner-wrap">
<h2 class="action-panel-heading">
Your saved search
</h2>
<form id="saved-search-action-panel-form"
class="saved-search-action-panel-form action-panel-content action-form"
data-create-saved-search-url="/create-saved-search/"
data-try-search-terms-url="/try-search-term/"
data-saved-search-root-url="https://www.ncbi.nlm.nih.gov/myncbi/searches/">
<input type="hidden" name="csrfmiddlewaretoken" value="Wvagi4pBKNgbPkim3itZiwMhtAW4U3ISdiUlVUSXko3FJLocGB61MEiV1EEgNEgc">
<div class="action-panel-control-wrap">
<label for="saved-search-name" class="action-panel-label saved-search-name-label required-field-asterisk">
Name of saved search:
</label>
<input maxlength="200"
type="text"
name="saved-search-name"
id="saved-search-name"
class="saved-search-name"
value=""
required
pattern="[^&quot;&amp;=&lt;&gt;\/]*" title="The following characters are not allowed in the Name field: &quot;&amp;=&lt;&gt;/">
</div>
<div class="action-panel-control-wrap">
<label for="saved-search-term" class="action-panel-label required-field-asterisk">
Search terms:
</label>
<textarea name="saved-search-term" id="saved-search-term" class="saved-search-term" required></textarea>
</div>
<div class="test-search-term-wrap">
<a href="#" class="try-search-term">Test search terms</a>
</div>
<div class="choice-group action-panel-extra-margin-top">
<span class="action-panel-label" id="fieldset-label">
Would you like email updates of new search results?
</span>
<fieldset id="saved-search-alert" aria-describedby="fieldset-label">
<legend class="usa-sr-only">Saved Search Alert Radio Buttons</legend>
<ul class="radio-group-items">
<li>
<input type="radio" id="saved-search-alert-yes" class="saved-search-alert-yes" name="saved-search-alert" value="yes" checked>
<label for="saved-search-alert-yes" class="action-panel-label">Yes</label>
</li>
<li>
<input aria-label="No radio input" type="radio" id="saved-search-alert-no" class="saved-search-alert-no" name="saved-search-alert" value="no">
<label for="saved-search-alert-no" class="action-panel-label">No</label>
</li>
</ul>
</fieldset>
</div>
<div class="alert-schedule-wrap">
<div class="action-panel-control-wrap">
<label class="action-panel-label">
Email:
</label>
<span aria-label="Email address" id="saved-search-email" class="action-panel-label"><span class="action-panel-label-bold"></span> (<a class="myncbi-account-settings" href="https://www.ncbi.nlm.nih.gov/account/settings/">change</a>)</span>
</div>
<div class="action-panel-control-wrap action-panel-extra-margin-top">
<label for="saved-search-frequency" class="action-panel-label">
Frequency:
</label>
<select id="saved-search-frequency" class="no-border-panel-selector saved-search-frequency">
<option value="monthly">Monthly</option>
<option value="weekly">Weekly</option>
<option value="daily">Daily</option>
</select>
</div>
<div class="action-panel-control-wrap saved-search-monthly-additional">
<label for="saved-search-monthly-on-day" class="action-panel-label">
Which day?
</label>
<select id="saved-search-monthly-on-day" class="no-border-panel-selector">
<option value="Sunday">The first Sunday</option>
<option value="Monday">The first Monday</option>
<option value="Tuesday">The first Tuesday</option>
<option value="Wednesday">The first Wednesday</option>
<option value="Thursday">The first Thursday</option>
<option value="Friday">The first Friday</option>
<option value="Saturday">The first Saturday</option>
<option value="day">The first day</option>
<option value="weekday">The first weekday</option>
</select>
</div>
<div class="action-panel-control-wrap saved-search-weekly-additional">
<label for="saved-search-weekly-on-day" class="action-panel-label">
Which day?
</label>
<select id="saved-search-weekly-on-day" class="no-border-panel-selector saved-search-weekly-on-day">
<option value="Sunday">Sunday</option>
<option value="Monday">Monday</option>
<option value="Tuesday">Tuesday</option>
<option value="Wednesday">Wednesday</option>
<option value="Thursday">Thursday</option>
<option value="Friday">Friday</option>
<option value="Saturday">Saturday</option>
</select>
</div>
<div class="action-panel-control-wrap">
<label for="saved-search-report" class="action-panel-label">
Report format:
</label>
<select id="saved-search-report" class="no-border-panel-selector saved-search-report">
<option value="DocSum">Summary</option>
<option value="DocSumText">Summary (text)</option>
<option value="Abstract">Abstract</option>
<option value="AbstractText">Abstract (text)</option>
<option value="MEDLINE">PubMed</option>
</select>
</div>
<div class="action-panel-control-wrap">
<label for="saved-search-amount" class="action-panel-label">
Send at most:
</label>
<select id="saved-search-amount" class="no-border-panel-selector saved-search-amount">
<option value="1">1 item</option>
<option value="5" selected>5 items</option>
<option value="10">10 items</option>
<option value="20">20 items</option>
<option value="50">50 items</option>
<option value="100">100 items</option>
<option value="200">200 items</option>
</select>
</div>
<div>
<input type="checkbox" id="saved-search-send-if-no-result" class="saved-search-send-if-no-result" name="saved-search-send-if-no-result">
<label for="saved-search-send-if-no-result" class="action-panel-label smaller-checkbox">
Send even when there aren't any new results
</label>
</div>
<div class="action-panel-control-wrap option-text-in-email-wrap">
<label for="saved-search-email-text" class="action-panel-label">
Optional text in email:
</label>
<textarea name="saved-search-email-text"
id="saved-search-email-text"
class="saved-search-email-text"></textarea>
</div>
</div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Saving..."
data-ga-category="save_share"
data-ga-action="alert"
data-ga-label="save">
Save
</button>
<button class="action-panel-cancel"
aria-label="Close 'Your saved search' panel"
ref="linksrc=close_saved_search_panel"
aria-controls="saved-search-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="alert"
data-ga-label="cancel">
Cancel
</button>
</div>
</form>
</div>
</div>
<div id="citation-manager-action-panel" class="citation-manager-action-panel action-panel" aria-hidden="true">
<div class="inner-wrap">
<h2 class="action-panel-heading">
Create a file for external citation management software
</h2>
<form id="citation-manager-action-panel-form"
class="action-panel-content action-form"
action="/results-export-ids/"
data-by-search-action="/results-export-search-data/"
data-by-ids-action="/results-export-ids/"
method="post"
data-by-search-method="post"
data-by-ids-method="post">
<input type="hidden" name="csrfmiddlewaretoken" value="Wvagi4pBKNgbPkim3itZiwMhtAW4U3ISdiUlVUSXko3FJLocGB61MEiV1EEgNEgc">
<input name="results-format" type="hidden" value="pubmed"/>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Sending..."
data-ga-category="save_share"
data-ga-action="citation_manager"
data-ga-label="save">
Create file
</button>
<button class="action-panel-cancel"
aria-label="Close 'Send citations to citation manager' panel"
ref="linksrc=close_citation_manager_panel"
aria-controls="citation-manager-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="citation_manager"
data-ga-label="cancel">
Cancel
</button>
</div>
</form>
</div>
</div>
<div id="rss-action-panel" class="rss-action-panel action-panel " aria-hidden="true">
<div class="inner-wrap">
<h2 class="action-panel-heading">
Your RSS Feed
</h2>
<form id="rss-action-panel-form"
class="rss-action-panel-form action-panel-content action-form"
data-create-rss-feed-url="/create-rss-feed-url/"
data-search-form-term-value="">
<input type="hidden" name="csrfmiddlewaretoken" value="Wvagi4pBKNgbPkim3itZiwMhtAW4U3ISdiUlVUSXko3FJLocGB61MEiV1EEgNEgc">
<div class="action-panel-control-wrap">
<label for="rss-name" class="action-panel-label required-field-asterisk">
Name of RSS Feed:
</label>
<input maxlength="200"
placeholder="Name"
type="text"
name="rss-name"
id="rss-name"
class="rss-name"
value=''
required
pattern="[^&quot;&amp;=&lt;&gt;\/]*" title="The following characters are not allowed in the Name field: &quot;&amp;=&lt;&gt;/">
</div>
<div class="rss-limit-wrap">
<div class="action-panel-control-wrap action-panel-extra-margin-top">
<label for="rss-limit" class="action-panel-label">
Number of items displayed:
</label>
<select id="rss-limit" class="no-border-panel-selector rss-limit">
<option value="5">5</option>
<option value="10">10</option>
<option value="15" selected="selected">15</option>
<option value="20">20</option>
<option value="50">50</option>
<option value="100">100</option>
</select>
</div>
</div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Creating..."
data-ga-category="save_share"
data-ga-action="alert"
data-ga-label="save">
Create RSS
</button>
<button class="action-panel-cancel"
aria-label="Close 'Your RSS' panel"
ref="linksrc=close_rss_panel"
aria-controls="rss-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="alert"
data-ga-label="cancel">
Cancel
</button>
</div>
<div class="action-panel-control-wrap rss-link-copy-wrap">
<label for="rss-link" class="usa-sr-only">RSS Link</label>
<input placeholder="Your RSS Feed Link" type="text" name="rss-link" id="rss-link" class="rss-link" title="RSS Link">
<button
type="button"
disabled
class="rss-link-copy-button disabled"
data-ga-category="save_share"
data-ga-action="rss"
data-ga-label="copy">
Copy
</button>
</div>
</form>
</div>
</div>
</div>
</div>
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<div class="full-text-links">
<div class="full-view">
<h3 class="title">
Full text links
</h3>
<div class="full-text-links-list">
<a class="link-item
dialog-focus"
href="https://journals.asm.org/doi/10.1128/JB.02542-14?url_ver=Z39.88-2003&amp;rfr_id=ori:rid:crossref.org&amp;rfr_dat=cr_pub 0pubmed"
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target="_blank"
rel="noopener"
ref="linksrc=fulltextorjournal_fulltext&amp;is_pmc=True&amp;PrId=3494&amp;itool=Abstract-def&amp;log$=linkouticon&amp;uid=25645563&amp;db=pubmed&amp;nlmid=2985120R"
title="Free full text at PubMed Central"
data-ga-category="full_text"
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Free PMC article
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</div>
<div class="short-view">
<a href="#" class="full-text-links-button full-text-links-dialog-trigger">
Full text links
</a>
</div>
</div>
<div class="actions-buttons sidebar"><h3 class="title">Actions</h3><div class="inner-wrap"><button class="citation-button citation-dialog-trigger"
aria-label="Open dialog with citation text in different styles"
data-ga-category="save_share"
data-ga-action="cite"
data-ga-label="open"
data-all-citations-url="/25645563/citations/"
data-citation-style="nlm"
data-pubmed-format-link="/25645563/export/"><span class="button-label">Cite</span></button><link type="text/css" href="ncbi-overlay-block/src/overlay-block.css"><div class="collections-button-container" data-article-id="25645563" data-article-db="pubmed"><button class="collections-button collections-dialog-trigger"
aria-label="Save article in MyNCBI collections."
data-ga-category="collections_button"
data-ga-action="click"
data-ga-label="collections_button"
data-collections-open-dialog-enabled="false"
data-collections-open-dialog-url="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F25645563%2F%23open-collections-dialog"
data-in-collections="false"><span class="button-label">Collections</span></button><div class="overlay" role="dialog"><div id="collections-action-dialog"
class="dialog collections-dialog"
aria-hidden="true"><div class="title">Add to Collections</div><div class="collections-action-panel action-panel"><form id="collections-action-dialog-form"
class="collections-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
data-existing-collections-url="/list-existing-collections/"
data-add-to-existing-collection-url="/add-to-existing-collection/"
data-create-and-add-to-new-collection-url="/create-and-add-to-new-collection/"
data-myncbi-max-collection-name-length="100"
data-collections-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/"><input type="hidden" name="csrfmiddlewaretoken" value="Wvagi4pBKNgbPkim3itZiwMhtAW4U3ISdiUlVUSXko3FJLocGB61MEiV1EEgNEgc"><div class="choice-group" role="radiogroup"><ul class="radio-group-items"><li><input type="radio"
id="collections-action-dialog-new"
class="collections-new"
name="collections"
value="new"
data-ga-category="collections_button"
data-ga-action="click"
data-ga-label="collections_radio_new"><label for="collections-action-dialog-new">Create a new collection</label></li><li><input type="radio"
id="collections-action-dialog-existing"
class="collections-existing"
name="collections"
value="existing"
checked="true"
data-ga-category="collections_button"
data-ga-action="click"
data-ga-label="collections_radio_existing"><label for="collections-action-dialog-existing">Add to an existing collection</label></li></ul></div><div class="controls-wrapper"><div class="action-panel-control-wrap new-collections-controls"><label for="collections-action-dialog-add-to-new" class="action-panel-label required-field-asterisk">
Name your collection:
</label><input
type="text"
name="add-to-new-collection"
id="collections-action-dialog-add-to-new"
class="collections-action-add-to-new"
pattern="[^&quot;&amp;=&lt;&gt;\/]*" title="The following characters are not allowed in the Name field: &quot;&amp;=&lt;&gt;/"
maxlength="100"
data-ga-category="collections_button"
data-ga-action="create_collection"
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devI is an evolutionarily young negative regulator of Myxococcus xanthus development
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Abstract
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<p>
During starvation-induced development of Myxococcus xanthus, thousands of rod-shaped cells form mounds in which they differentiate into spores. The dev locus includes eight genes followed by clustered regularly interspaced short palindromic repeats (CRISPRs), comprising a CRISPR-Cas system (Cas stands for CRISPR associated) typically involved in RNA interference. Mutations in devS or devR of a lab reference strain permit mound formation but impair sporulation. We report that natural isolates of M. xanthus capable of normal development are highly polymorphic in the promoter region of the dev operon. We show that the dev promoter is predicted to be nonfunctional in most natural isolates and is dispensable for development of a laboratory reference strain. Moreover, deletion of the dev promoter or the small gene immediately downstream of it, here designated devI (development inhibitor), suppressed the sporulation defect of devS or devR mutants in the lab strain. Complementation experiments and the result of introducing a premature stop codon in devI support a model in which DevRS proteins negatively autoregulate expression of devI, whose 40-residue protein product DevI inhibits sporulation if overexpressed. DevI appears to act in a cell-autonomous manner since experiments with conditioned medium and with cell mixtures gave no indication of extracellular effects. Strikingly, we report that devI is entirely absent from most M. xanthus natural isolates and was only recently integrated into the developmental programs of some lineages. These results provide important new insights into both the evolutionary history of the dev operon and its mechanistic role in M. xanthus sporulation.
</p>
<p>
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Importance:
</strong>
Certain mutations in the dev CRISPR-Cas (clustered regularly interspaced short palindromic repeat-associated) system of Myxococcus xanthus impair sporulation. The link between development and a CRISPR-Cas system has been a mystery. Surprisingly, DNA sequencing of natural isolates revealed that many appear to lack a functional dev promoter, yet these strains sporulate normally. Deletion of the dev promoter or the small gene downstream of it suppressed the sporulation defect of a lab strain with mutations in dev genes encoding Cas proteins. The results support a model in which the Cas proteins DevRS prevent overexpression of the small gene devI, which codes for an inhibitor of sporulation. Phylogenetic analysis of natural isolates suggests that devI and the dev promoter were only recently acquired in some lineages.
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Copyright © 2015, American Society for Microbiology. All Rights Reserved.
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<strong class="figure-label">
<p> FIG 1 </p>
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<div class="figure-caption-contents"><p> Map of the M. xanthus… </p></div>
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<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> FIG 1 </p>
</strong>
<div class="figure-caption-contents"><p> Map of the M. xanthus laboratory strain DK1622 <i> dev </i> operon and structural evolution… </p></div>
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<figcaption id="figure-caption-0" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
FIG 1
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<div class="figure-caption-contents">Map of the M. xanthus laboratory strain DK1622 <i>dev</i> operon and structural evolution of the <i>dev</i> promoter region among natural lineages. (A) Map of the DK1622 <i>dev</i> operon and expanded view of the <i>dev</i> promoter region. The top part depicts the eight genes of the <i>dev</i> operon, which also includes at least two repeats of the downstream CRISPR. The expanded view shows the region of some natural isolates that was subjected to Sanger sequencing (sequences are shown in Fig. S1 in the supplemental material). This region includes the <i>dev</i> promoter and the small gene <i>devI</i>. Numbers are relative to the transcriptional start site (+1), and a bent arrow indicates the direction of transcription. (B) Structure and evolution of the <i>dev</i> promoter region. The leftward part shows phylogenetic relationships among natural isolates inferred from 4.5 Mbp of orthologous sequence. M. fulvus HW-1 (52) served as the outgroup. Bootstrap values supporting branch inferences are shown near each branch. The center part shows the structure of the <i>dev</i> promoter region. Black boxes highlight orthologous regions shared among natural isolates and the reference strain DK1622. Thin lines depict DK1622 sequence regions that are absent from the respective genomes, either because there is no sequence at all in the corresponding region or because the sequence that is present is nonorthologous to that of DK1622. The rightward part shows a phylogenetic tree of a conserved partial segment of MXAN_7267 highlighting recent evolutionary history of the orthologous coding region upstream of the <i>dev</i> promoter. Bootstrap values larger than 60% are shown at the respective nodes. Filled circles indicate strains identified by the horizontally corresponding strain in the leftward phylogeny, whereas open circles identify strains found at a different horizontal level in the leftward phylogeny. Note that the topological structures of MXAN_7267- and whole-genome-based trees are divergent. Branches of the MXAN_7267 tree were rotated around nodes to maximize horizontal alignment to the genome-based phylogeny, but these rotations did not alter tree structure. The asterisk on the branch leading to Chihaya 20 represents the most likely branch position of DK897 in the MXAN_7267 tree, based on the available sequence information for DK897 (see Fig. S1 in the supplemental material), which covered significantly less of the conserved partial segment of MXAN_7267 than it did for the other strains and therefore was not used in the tree construction.</div>
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itemprop="contentUrl"
aria-describedby="figure-caption-1"
role="button"
data-image-width="750"
data-image-height="801"
data-image-alt="FIG 2"
data-pmc-id="PMC4352663"
data-figure-id="F2">
<img class="figure-thumb" itemprop="thumbnail"
id="article-image-1"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/68e9/4352663/5142626e4cb6/zjb9990935540002.gif"
alt="FIG 2" />
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<div class="caption-wrap">
<strong class="figure-label">
<p> FIG 2 </p>
</strong>
<div class="figure-caption-contents"><p> Development of <i> dev </i> mutants under… </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> FIG 2 </p>
</strong>
<div class="figure-caption-contents"><p> Development of <i> dev </i> mutants under submerged culture conditions. (A) Fruiting body formation by… </p></div>
</div>
<figcaption id="figure-caption-1" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
FIG 2
</strong>
<div class="figure-caption-contents">Development of <i>dev</i> mutants under submerged culture conditions. (A) Fruiting body formation by the laboratory strain DK1622 and the indicated <i>dev</i> mutants. Dark fruiting bodies are observed at 96 h into development of DK1622 (an arrow points to one) but not the <i>dev</i> mutants. Bar, 100 μm. Similar results were observed in at least two biological replicates. (B) Cellular shape change. Developing cultures were subjected to gentle dispersion and examined microscopically at the indicated times. Photos show densely packed cell aggregates presumed to be nascent fruiting bodies. Arrows point to round or ovoid cells. Bar, 5 μm. Similar results were observed in at least two biological replicates. (C) Sporulation. Samples were harvested at 72 h into development for measurement of mature spores. Values (log<sub>10</sub>) are the averages from at least three biological replicates, and error bars represent 1 standard deviation from the mean.</div>
</figcaption>
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data-image-width="800"
data-image-height="368"
data-image-alt="FIG 3"
data-pmc-id="PMC4352663"
data-figure-id="F3">
<img class="figure-thumb" itemprop="thumbnail"
id="article-image-2"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/68e9/4352663/9e12c7719ca9/zjb9990935540003.gif"
alt="FIG 3" />
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<strong class="figure-label">
<p> FIG 3 </p>
</strong>
<div class="figure-caption-contents"><p> Development of ΔP <sub> <i> dev </i> </sub> and… </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> FIG 3 </p>
</strong>
<div class="figure-caption-contents"><p> Development of ΔP <sub> <i> dev </i> </sub> and Δ <i> devI </i> mutants. Fruiting body formation by the… </p></div>
</div>
<figcaption id="figure-caption-2" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
FIG 3
</strong>
<div class="figure-caption-contents">Development of ΔP<sub><i>dev</i></sub> and Δ<i>devI</i> mutants. Fruiting body formation by the laboratory strain DK1622 and the indicated mutants under submerged culture conditions. Arrows point to dark fruiting bodies observed at 72 h poststarvation for DK1622 and several of the mutants. Bar, 100 μm. Similar results were observed in at least two biological replicates.</div>
</figcaption>
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<figure class="figure-item "
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itemprop="contentUrl"
aria-describedby="figure-caption-3"
role="button"
data-image-width="680"
data-image-height="332"
data-image-alt="FIG 4"
data-pmc-id="PMC4352663"
data-figure-id="F4">
<img class="figure-thumb" itemprop="thumbnail"
id="article-image-3"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/68e9/4352663/6370a25316d9/zjb9990935540004.gif"
alt="FIG 4" />
</a>
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<div class="caption-wrap">
<strong class="figure-label">
<p> FIG 4 </p>
</strong>
<div class="figure-caption-contents"><p> Levels of <i> dev </i> transcripts. (A)… </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> FIG 4 </p>
</strong>
<div class="figure-caption-contents"><p> Levels of <i> dev </i> transcripts. (A) Comparison of the laboratory strain DK1622 with the… </p></div>
</div>
<figcaption id="figure-caption-3" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
FIG 4
</strong>
<div class="figure-caption-contents">Levels of <i>dev</i> transcripts. (A) Comparison of the laboratory strain DK1622 with the ΔP<sub><i>dev</i></sub> mutant. At 24 h poststarvation under submerged culture conditions, cultures were harvested, RNA was isolated, and the RNA was subjected to qRT-PCR analysis using primers Pdev-T-F and Pdev-T-R, designed to amplify the region from +4811 to +4940 relative to the transcriptional start site of the <i>dev</i> operon. (B) Comparison of DK1622 with the Δ<i>devS</i> and Δ<i>devR</i> mutants. Culture conditions were as described for panel A. RNA was subjected to qRT-PCR analysis using primers PdevF-2 and PdevR-3, designed to amplify the region from +237 to +440 relative to the <i>dev</i> transcriptional start site. For both panels, values are the averages of three technical replicates for at least three biological replicates and are reported relative to DK1622. Error bars indicate 1 standard deviation from the mean.</div>
</figcaption>
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itemprop="contentUrl"
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role="button"
data-image-width="742"
data-image-height="786"
data-image-alt="FIG 5"
data-pmc-id="PMC4352663"
data-figure-id="F5">
<img class="figure-thumb" itemprop="thumbnail"
id="article-image-4"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/68e9/4352663/d82c6c89c3fe/zjb9990935540005.gif"
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</a>
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<strong class="figure-label">
<p> FIG 5 </p>
</strong>
<div class="figure-caption-contents"><p> Complementation of the Δ <i> devI… </i> </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> FIG 5 </p>
</strong>
<div class="figure-caption-contents"><p> Complementation of the Δ <i> devI </i> Δ <i> devS </i> double mutant. (A) Map of the… </p></div>
</div>
<figcaption id="figure-caption-4" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
FIG 5
</strong>
<div class="figure-caption-contents">Complementation of the Δ<i>devI</i> Δ<i>devS</i> double mutant. (A) Map of the <i>dev</i> promoter region and fragments used for complementation. Boxes indicate genes. Numbers are relative to the transcriptional start site (+1), and a bent arrow indicates the direction of transcription. Lines below the map indicate fragments used for complementation. (B) Fruiting body formation by the laboratory strain DK1622 and the indicated mutants under submerged culture conditions. Endpoints of complementing segments relative to the <i>dev</i> transcriptional start site are indicated in parentheses. Arrows point to dark fruiting bodies observed at 72 h poststarvation for DK1622 and several of the mutants. Bar, 100 μm. Similar results were observed in at least two biological replicates. (C) Sporulation. Samples were harvested at 72 h into development for measurement of mature spores. Values (log<sub>10</sub>) are the averages from at least three biological replicates, and error bars represent 1 standard deviation from the mean. (D) Levels of <i>dev</i> transcripts. At 24 h poststarvation under submerged culture conditions, cultures were harvested, RNA was isolated, and the RNA was subjected to qRT-PCR analysis using primers 7266-F and 7266-R, designed to amplify the region from +36 to +159. Values are the averages from three technical replicates for at least three biological replicates and are reported relative to DK1622. Error bars indicate 1 standard deviation from the mean.</div>
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<img class="figure-thumb" itemprop="thumbnail"
id="article-image-5"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/68e9/4352663/189b6b7183d2/zjb9990935540006.gif"
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<strong class="figure-label">
<p> FIG 6 </p>
</strong>
<div class="figure-caption-contents"><p> Effects of a premature stop… </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> FIG 6 </p>
</strong>
<div class="figure-caption-contents"><p> Effects of a premature stop codon in <i> devI </i> . (A) Fruiting body formation… </p></div>
</div>
<figcaption id="figure-caption-5" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
FIG 6
</strong>
<div class="figure-caption-contents">Effects of a premature stop codon in <i>devI</i>. (A) Fruiting body formation by the laboratory strain DK1622 and the indicated mutants under submerged culture conditions. <i>devI-STOP</i> indicates the single-base-pair insertion that creates an in-frame stop codon. Arrows point to dark fruiting bodies observed at 72 h poststarvation. Bar, 100 μm. Similar results were observed in at least two biological replicates. (B) Sporulation. Samples were harvested at 96 h into development for measurement of mature spores. Values (log<sub>10</sub>) are the averages from at least three biological replicates, and error bars represent 1 standard deviation from the mean.</div>
</figcaption>
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<strong class="figure-label">
<p> FIG 7 </p>
</strong>
<div class="figure-caption-contents"><p> Effect of conditioned starvation buffer… </p></div>
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</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> FIG 7 </p>
</strong>
<div class="figure-caption-contents"><p> Effect of conditioned starvation buffer from the Δ <i> devS </i> mutant on development of… </p></div>
</div>
<figcaption id="figure-caption-6" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
FIG 7
</strong>
<div class="figure-caption-contents">Effect of conditioned starvation buffer from the Δ<i>devS</i> mutant on development of the laboratory strain DK1622 and effect of codevelopment of the Δ<i>devS</i> mutant with DK1622. (A) Overlying conditioned starvation buffer from the Δ<i>devS</i> mutant at 18, 24, or 30 h under submerged culture conditions was used to replace the overlying buffer of comparably treated DK1622 at 18 or 24 h poststarvation (e.g., 24-18 means the conditioned overlay from Δ<i>devS</i> at 24 h was used to replace the overlay of DK1622 at 18 h). Samples collected at 30 and 36 h poststarvation (left and right bars, respectively, for each replacement regimen) were sonicated, and spores were quantified microscopically using a Neubauer counting chamber. Values (log<sub>10</sub>) are the averages from at least three biological replicates. Error bars represent 1 standard deviation from the mean. (B) Effect of codevelopment on fruiting body formation. A derivative of strain DK1622 with a kanamycin resistance marker (DK1622 Km<sup>r</sup>), the Δ<i>devS</i> mutant, and mixtures of the two strains at the indicated ratios were subjected to starvation under submerged culture conditions. Arrows point to dark fruiting bodies observed at 96 h poststarvation. Bar, 100 μm. Similar results were observed in at least two biological replicates. (C) Effect of codevelopment on sporulation. Samples were harvested at 96 h for the measurement of mature spores. Values (log<sub>10</sub>) are the averages from at least three biological replicates, and error bars represent 1 standard deviation from the mean.</div>
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