The significance of nitrogen cost minimization in proteomes of marine microorganisms
Identifieur interne : 000465 ( Pmc/Checkpoint ); précédent : 000464; suivant : 000466The significance of nitrogen cost minimization in proteomes of marine microorganisms
Auteurs : Joseph J. Grzymski [États-Unis] ; Alex M. Dussaq [États-Unis]Source :
- The ISME Journal [ 1751-7362 ] ; 2011.
Abstract
Marine microorganisms thrive under low levels of nitrogen (N). N cost minimization is a major selective pressure imprinted on open-ocean microorganism genomes. Here we show that amino-acid sequences from the open ocean are reduced in N, but increased in average mass compared with coastal-ocean microorganisms. Nutrient limitation exerts significant pressure on organisms supporting the trade-off between N cost minimization and increased average mass of amino acids that is a function of increased A+T codon usage. N cost minimization, especially of highly expressed proteins, reduces the total cellular N budget by 2.7–10% this minimization in combination with reduction in genome size and cell size is an evolutionary adaptation to nutrient limitation. The biogeochemical and evolutionary precedent for these findings suggests that N limitation is a stronger selective force in the ocean than biosynthetic costs and is an important evolutionary strategy in resource-limited ecosystems.
Url:
DOI: 10.1038/ismej.2011.72
PubMed: 21697958
PubMed Central: 3246230
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>Marine microorganisms thrive under low levels of nitrogen (N). N cost minimization is a major selective pressure imprinted on open-ocean microorganism genomes. Here we show that amino-acid sequences from the open ocean are reduced in N, but increased in average mass compared with coastal-ocean microorganisms. Nutrient limitation exerts significant pressure on organisms supporting the trade-off between N cost minimization and increased average mass of amino acids that is a function of increased A+T codon usage. N cost minimization, especially of highly expressed proteins, reduces the total cellular N budget by 2.7–10% this minimization in combination with reduction in genome size and cell size is an evolutionary adaptation to nutrient limitation. The biogeochemical and evolutionary precedent for these findings suggests that N limitation is a stronger selective force in the ocean than biosynthetic costs and is an important evolutionary strategy in resource-limited ecosystems.</p>
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<journal-title-group><journal-title>The ISME Journal</journal-title>
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<issn pub-type="ppub">1751-7362</issn>
<issn pub-type="epub">1751-7370</issn>
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<article-meta><article-id pub-id-type="pmid">21697958</article-id>
<article-id pub-id-type="pmc">3246230</article-id>
<article-id pub-id-type="pii">ismej201172</article-id>
<article-id pub-id-type="doi">10.1038/ismej.2011.72</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject>
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<title-group><article-title>The significance of nitrogen cost minimization in proteomes of marine microorganisms</article-title>
<alt-title alt-title-type="running">Nitrogen cost minimization in marine microbes</alt-title>
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<contrib-group><contrib contrib-type="author"><name><surname>Grzymski</surname>
<given-names>Joseph J</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="corresp" rid="caf1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dussaq</surname>
<given-names>Alex M</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<aff id="aff1"><label>1</label>
<institution>Division of Earth and Ecosystem Sciences, Desert Research Institute</institution>
, Reno, NV,<country>USA</country>
</aff>
</contrib-group>
<author-notes><corresp id="caf1"><label>*</label>
<institution>Division of Earth and Ecosystem Studies, Desert Research Institute</institution>
, 2215 Raggio Parkway, Reno, NV 89512, <country>USA</country>
. E-mail: <email>joeg@dri.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub"><month>01</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>23</day>
<month>06</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>1</day>
<month>1</month>
<year>2012</year>
</pub-date>
<volume>6</volume>
<issue>1</issue>
<fpage>71</fpage>
<lpage>80</lpage>
<history><date date-type="received"><day>25</day>
<month>01</month>
<year>2011</year>
</date>
<date date-type="rev-recd"><day>30</day>
<month>03</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>26</day>
<month>04</month>
<year>2011</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2012 International Society for Microbial Ecology</copyright-statement>
<copyright-year>2012</copyright-year>
<copyright-holder>International Society for Microbial Ecology</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under the Creative Commons Attribution-NonCommercial-No Derivative Works 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/</license-p>
</license>
</permissions>
<abstract><p>Marine microorganisms thrive under low levels of nitrogen (N). N cost minimization is a major selective pressure imprinted on open-ocean microorganism genomes. Here we show that amino-acid sequences from the open ocean are reduced in N, but increased in average mass compared with coastal-ocean microorganisms. Nutrient limitation exerts significant pressure on organisms supporting the trade-off between N cost minimization and increased average mass of amino acids that is a function of increased A+T codon usage. N cost minimization, especially of highly expressed proteins, reduces the total cellular N budget by 2.7–10% this minimization in combination with reduction in genome size and cell size is an evolutionary adaptation to nutrient limitation. The biogeochemical and evolutionary precedent for these findings suggests that N limitation is a stronger selective force in the ocean than biosynthetic costs and is an important evolutionary strategy in resource-limited ecosystems.</p>
</abstract>
<kwd-group><kwd>amino-acid usage</kwd>
<kwd>cost minimization</kwd>
<kwd>oligotrophy</kwd>
<kwd>nitrogen</kwd>
<kwd>resource limitation</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Figure 1</label>
<caption><p>Annual 10 m nitrate concentration for world oceans. Red dots are GOS sampling sites used in our analyses.</p>
</caption>
<graphic xlink:href="ismej201172f1"></graphic>
</fig>
<fig id="fig2"><label>Figure 2</label>
<caption><p>Nitrogens per amino-acid residue side chain for GOS environmental genome data. (<bold>a</bold>
) Quantile plots of the average number of nitrogen ARSC for GOS stations. Red lines represent coastal-ocean sites from the GOS data set as defined in Materials and methods. Blue lines are from open-ocean sites. (<bold>b</bold>
) The median N ARSC for each GOS site and one from a sewage metagenome. The color reproduction of this figure is available at the <italic>ISME Journal</italic>
online.</p>
</caption>
<graphic xlink:href="ismej201172f2"></graphic>
</fig>
<fig id="fig3"><label>Figure 3</label>
<caption><p>Median nitrogen ARSC as it correlates to proximity of landmass. The correlation between the nearest land mass and median N ARSC for each GOS metagenome station. Spearman correlation coefficients are presented in <xref ref-type="supplementary-material" rid="sup1">Supplementary Table S1</xref>
.</p>
</caption>
<graphic xlink:href="ismej201172f3"></graphic>
</fig>
<fig id="fig4"><label>Figure 4</label>
<caption><p>Circular genome plots of <italic>Prochlorococcus marinus</italic>
ecotypes. (<bold>a</bold>
) Coding (gray) and non-coding regions (red=leading strand, blue=lagging strand) for the <italic>P. marinus</italic>
ecotype MIT 9313. Additional data are available in <xref ref-type="supplementary-material" rid="sup1">Supplementary Tables S4 and S5c</xref>
. Averaged nitrogen ARSC for each ORF is plotted as a colored bar graph, with green indicating high nitrogen ARSC and red indicating lower as in Materials and methods. The concentric rings scale represents an increase of 0.03 N ARSC. (<bold>b</bold>
) As in (<bold>a</bold>
), but for the <italic>P. marinus</italic>
ecotype CCMP 1986. (<bold>c</bold>
) As in <bold>a</bold>
, but bar graphs represent subtraction of strain MIT9313—CCMP1986 N ARSC values for all genes in the core genome (1286) excluding hypothetical proteins. Green indicates positive values and red indicates negative values. The concentric rings scale represents changes of 0.03 N ARSC. (<bold>d</bold>
) Same as <bold>c</bold>
except representing the average amino-acid mass difference for strain MIT9313—CCMP1986. The concentric rings scale represents changes of 3 g mol<sup>−1</sup>
.</p>
</caption>
<graphic xlink:href="ismej201172f4"></graphic>
</fig>
<table-wrap id="tbl1"><label>Table 1</label>
<caption><title>Protein requirements in theoretical marine microorganism populations determined by modeling</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="char" char="±"></col>
<col align="char" char="±"></col>
<col align="char" char="±"></col>
<col align="char" char="±"></col>
<col align="char" char="±"></col>
<col align="char" char="±"></col>
<col align="char" char="±"></col>
<col align="char" char="±"></col>
<col align="char" char="±"></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><italic>Description</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>Cell size (μm<sup>3</sup>
)</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>Genome size (Mb)</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>G+C (%)</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>Total protein mass (fg cell</italic>
<sup><italic>−1</italic>
</sup>
<italic>)</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>N ARSC</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>Average mass (g mol</italic>
<sup><italic>−1</italic>
</sup>
<italic>)</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>Nitrogen requirement for protein (fmol cell</italic>
<sup><italic>−1</italic>
</sup>
<italic>)</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>Nitrogen requirement for DNA (fmol cell</italic>
<sup><italic>−1</italic>
</sup>
<italic>)</italic>
</th>
<th align="char" valign="top" char="±" charoff="50"><italic>Nitrogen requirement for protein+DNA (fmol cell</italic>
<sup><italic>−1</italic>
</sup>
<italic>)</italic>
</th>
</tr>
</thead>
<tbody valign="top"><tr><td align="left" valign="top" charoff="50">Average open ocean</td>
<td align="char" valign="top" char="±" charoff="50">0.0488±0.0008</td>
<td align="char" valign="top" char="±" charoff="50">2.01±0.01</td>
<td align="char" valign="top" char="±" charoff="50">34.0±0.2</td>
<td align="char" valign="top" char="±" charoff="50">14.833±0.145</td>
<td align="char" valign="top" char="±" charoff="50">0.3377±0.0002</td>
<td align="char" valign="top" char="±" charoff="50">113.03±0.04</td>
<td align="char" valign="top" char="±" charoff="50">34.443±0.337</td>
<td align="char" valign="top" char="±" charoff="50">4.802±0.029</td>
<td align="char" valign="top" char="±" charoff="50">39.245±0.346</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Open-ocean high G+C</td>
<td align="char" valign="top" char="±" charoff="50">0.0495±0.0007</td>
<td align="char" valign="top" char="±" charoff="50">2.00±0.01</td>
<td align="char" valign="top" char="±" charoff="50">49.9±0.2</td>
<td align="char" valign="top" char="±" charoff="50">14.941±0.130</td>
<td align="char" valign="top" char="±" charoff="50">0.3521±0.0002</td>
<td align="char" valign="top" char="±" charoff="50">110.62±0.03</td>
<td align="char" valign="top" char="±" charoff="50">35.831±0.308</td>
<td align="char" valign="top" char="±" charoff="50">4.898±0.036</td>
<td align="char" valign="top" char="±" charoff="50">40.729±0.304</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Open-ocean high cell volume</td>
<td align="char" valign="top" char="±" charoff="50">0.0634±0.0011</td>
<td align="char" valign="top" char="±" charoff="50">2.00±0.01</td>
<td align="char" valign="top" char="±" charoff="50">34.1±0.3</td>
<td align="char" valign="top" char="±" charoff="50">17.282±0.180</td>
<td align="char" valign="top" char="±" charoff="50">0.3378±0.0003</td>
<td align="char" valign="top" char="±" charoff="50">113.02±0.05</td>
<td align="char" valign="top" char="±" charoff="50">40.138±0.425</td>
<td align="char" valign="top" char="±" charoff="50">4.785±0.033</td>
<td align="char" valign="top" char="±" charoff="50">44.923±0.435</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Open-ocean large genome size</td>
<td align="char" valign="top" char="±" charoff="50">0.0491±0.0008</td>
<td align="char" valign="top" char="±" charoff="50">3.90±0.01</td>
<td align="char" valign="top" char="±" charoff="50">34.1±0.2</td>
<td align="char" valign="top" char="±" charoff="50">14.875±0.130</td>
<td align="char" valign="top" char="±" charoff="50">0.3377±0.0002</td>
<td align="char" valign="top" char="±" charoff="50">113.02±0.04</td>
<td align="char" valign="top" char="±" charoff="50">34.543±0.313</td>
<td align="char" valign="top" char="±" charoff="50">9.332±0.027</td>
<td align="char" valign="top" char="±" charoff="50">43.875±0.306</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Ideal open ocean</td>
<td align="char" valign="top" char="±" charoff="50">0.0103±0.0002</td>
<td align="char" valign="top" char="±" charoff="50">2.01±0.02</td>
<td align="char" valign="top" char="±" charoff="50">34.1±0.3</td>
<td align="char" valign="top" char="±" charoff="50">5.929±0.060</td>
<td align="char" valign="top" char="±" charoff="50">0.3378±0.0003</td>
<td align="char" valign="top" char="±" charoff="50">113.02±0.05</td>
<td align="char" valign="top" char="±" charoff="50">13.769±0.142</td>
<td align="char" valign="top" char="±" charoff="50">4.796±0.044</td>
<td align="char" valign="top" char="±" charoff="50">18.565±0.169</td>
</tr>
<tr><td align="left" valign="top" charoff="50">‘Coastal' ocean</td>
<td align="char" valign="top" char="±" charoff="50">0.0635±0.0009</td>
<td align="char" valign="top" char="±" charoff="50">3.90±0.02</td>
<td align="char" valign="top" char="±" charoff="50">49.9±0.3</td>
<td align="char" valign="top" char="±" charoff="50">17.303±0.140</td>
<td align="char" valign="top" char="±" charoff="50">0.3521±0.0002</td>
<td align="char" valign="top" char="±" charoff="50">110.62±0.04</td>
<td align="char" valign="top" char="±" charoff="50">41.495±0.330</td>
<td align="char" valign="top" char="±" charoff="50">9.526±0.040</td>
<td align="char" valign="top" char="±" charoff="50">51.021±0.318</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t1-fn1"><p>Abbreviations: ARSC, atoms per residue side chain; N, nitrogen.</p>
</fn>
<fn id="t1-fn2"><p>Parameters and calculations based on observed relationships and previously published data as described in Materials and methods.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>États-Unis</li>
</country>
</list>
<tree><country name="États-Unis"><noRegion><name sortKey="Grzymski, Joseph J" sort="Grzymski, Joseph J" uniqKey="Grzymski J" first="Joseph J" last="Grzymski">Joseph J. Grzymski</name>
</noRegion>
<name sortKey="Dussaq, Alex M" sort="Dussaq, Alex M" uniqKey="Dussaq A" first="Alex M" last="Dussaq">Alex M. Dussaq</name>
</country>
</tree>
</affiliations>
</record>
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