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Transporter genes in biosynthetic gene clusters predict metabolite characteristics and siderophore activity
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class="contributor" id="contrib-1" itemprop="author" itemscope="itemscope" itemtype="http://schema.org/Person"><span class="name" itemprop="name"><a class="name-search" href="/search?author1=Alexander+Crits-Christoph&sortspec=date&submit=Submit">Alexander Crits-Christoph</a></span><a id="xref-aff-1-1" class="xref-aff" href="#aff-1">1</a><span class="xref-sep">,</span><a id="xref-aff-2-1" class="xref-aff" href="#aff-2">2</a>, </li> <li class="contributor" id="contrib-2" itemprop="author" itemscope="itemscope" itemtype="http://schema.org/Person"><span class="name" itemprop="name"><a class="name-search" href="/search?author1=Nicholas+Bhattacharya&sortspec=date&submit=Submit">Nicholas Bhattacharya</a></span><a id="xref-aff-3-1" class="xref-aff" href="#aff-3">3</a>, </li> <li class="contributor" id="contrib-3" itemprop="author" itemscope="itemscope" itemtype="http://schema.org/Person"><span class="name" itemprop="name"><a class="name-search" href="/search?author1=Matthew+R.+Olm&sortspec=date&submit=Submit">Matthew R. Olm</a></span><a id="xref-aff-4-1" class="xref-aff" href="#aff-4">4</a>, </li> <li class="contributor" id="contrib-4" itemprop="author" itemscope="itemscope" itemtype="http://schema.org/Person"><span class="name" itemprop="name"><a class="name-search" href="/search?author1=Yun+S.+Song&sortspec=date&submit=Submit">Yun S. Song</a></span><a id="xref-aff-5-1" class="xref-aff" href="#aff-5">5</a><span class="xref-sep">,</span><a id="xref-aff-6-1" class="xref-aff" href="#aff-6">6</a><span class="xref-sep">,</span><a id="xref-aff-7-1" class="xref-aff" href="#aff-7">7</a> and </li> <li class="last" id="contrib-5"><span class="name"><a class="name-search" href="/search?author1=Jillian+F.+Banfield&sortspec=date&submit=Submit">Jillian F. Banfield</a></span><a id="xref-aff-2-2" class="xref-aff" href="#aff-2">2</a><span class="xref-sep">,</span><a id="xref-aff-4-2" class="xref-aff" href="#aff-4">4</a><span class="xref-sep">,</span><a id="xref-aff-7-2" class="xref-aff" href="#aff-7">7</a><span class="xref-sep">,</span><a id="xref-aff-8-1" class="xref-aff" href="#aff-8">8</a><span class="xref-sep">,</span><a id="xref-aff-9-1" class="xref-aff" href="#aff-9">9</a></li> </ol> <ol class="affiliation-list"> <li class="aff"><a id="aff-1" name="aff-1"></a><address><sup>1</sup>Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA; </address> </li> <li class="aff"><a id="aff-2" name="aff-2"></a><address><sup>2</sup>Innovative Genomics Institute, Berkeley, California 94720, USA; </address> </li> <li class="aff"><a id="aff-3" name="aff-3"></a><address><sup>3</sup>Department of Mathematics, University of California, Berkeley, California 94720, USA; </address> </li> <li class="aff"><a id="aff-4" name="aff-4"></a><address><sup>4</sup>Department of Microbiology and Immunology, Stanford University, California 94305, USA; </address> </li> <li class="aff"><a id="aff-5" name="aff-5"></a><address><sup>5</sup>Department of Electrical Engineering and Computer Sciences, University of California, Berkeley, California 94720, USA; </address> </li> <li class="aff"><a id="aff-6" name="aff-6"></a><address><sup>6</sup>Department of Statistics, University of California, Berkeley, California 94720, USA; </address> </li> <li class="aff"><a id="aff-7" name="aff-7"></a><address><sup>7</sup>Chan Zuckerberg Biohub, San Francisco, California 94158, USA; </address> </li> <li class="aff"><a id="aff-8" name="aff-8"></a><address><sup>8</sup>Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720, USA; </address> </li> <li class="aff"><a id="aff-9" name="aff-9"></a><address><sup>9</sup>Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA </address> </li> </ol> </div> <li class="corresp" id="corresp-1">Corresponding author: <span class="em-link"><span class="em-addr">jbanfield{at}berkeley.edu</span></span></li> <div class="section abstract" id="abstract-1" itemprop="description"> <h2>Abstract</h2> <p id="p-2">Biosynthetic gene clusters (BGCs) are operonic sets of microbial genes that synthesize specialized metabolites with diverse functions, including siderophores and antibiotics, which often require export to the extracellular environment. For this reason, genes for transport across cellular membranes are essential for the production of specialized metabolites and are often genomically colocalized with BGCs. Here, we conducted a comprehensive computational analysis of transporters associated with characterized BGCs. In addition to known exporters, in BGCs we found many importer-specific transmembrane domains that co-occur with substrate binding proteins possibly for uptake of siderophores or metabolic precursors. Machine learning models using transporter gene frequencies were predictive of known siderophore activity, molecular weights, and a measure of lipophilicity (log <em>P</em>) for corresponding BGC-synthesized metabolites. Transporter genes associated with BGCs were often equally or more predictive of metabolite features than biosynthetic genes. Given the importance of siderophores as pathogenicity factors, we used transporters specific for siderophore BGCs to identify both known and uncharacterized siderophore-like BGCs in genomes from metagenomes from the infant and adult gut microbiome. We find that 23% of microbial genomes from premature infant guts have siderophore-like BGCs, but only 3% of those assembled from adult gut microbiomes do. Although siderophore-like BGCs from the infant gut are predominantly associated with Enterobacteriaceae and <em>Staphylococcus</em>, siderophore-like BGCs can be identified from taxa in the adult gut microbiome that have rarely been recognized for siderophore production. Taken together, these results show that consideration of BGC-associated transporter genes can inform predictions of specialized metabolite structure and function. </p> </div> <div class="section fn-group" id="fn-group-1"> <h2>Footnotes</h2> <ul> <li class="fn-supplementary-material" id="fn-1"> <p id="p-49">[Supplemental material is available for this article.]</p> </li> <li class="fn" id="fn-2"> <p id="p-50">Article published online before print. Article, supplemental material, and publication date are at <a href="http://www.genome.org/cgi/doi/10.1101/gr.268169.120">http://www.genome.org/cgi/doi/10.1101/gr.268169.120</a>. </p> </li> <li class="fn" id="fn-3"> <p id="p-51">Freely available online through the <em>Genome Research</em> Open Access option. </p> </li> </ul> </div> <ul class="history-list"> <li xmlns:hwp="http://schema.highwire.org/Journal" class="received" hwp:start="2020-06-30"><span class="received-label">Received </span>June 30, 2020. </li> <li xmlns:hwp="http://schema.highwire.org/Journal" class="accepted" hwp:start="2020-12-16"><span class="accepted-label">Accepted </span>December 16, 2020. </li> </ul> <ul class="copyright-statement"> <li class="fn" id="copyright-statement-1"><a href="/site/misc/terms.xhtml">漏 2021 Crits-Christoph et al.; Published by Cold Spring Harbor Laboratory Press</a></li> </ul> <div class="license" id="license-1"> <p id="p-1">This article, published in <em>Genome Research</em>, is 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