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Evolution of divergent life history strategies in marine alphaproteobacteria.

Luo H, Csuros M, Hughes AL, Moran MA - MBio (2013)

Bottom Line: The timing of the first Roseobacter genome expansion was coincident with the predicted radiation of modern marine eukaryotic phytoplankton of sufficient size to create nutrient-enriched microzones and is consistent with present-day ecological associations between these microbial groups.We suggest that diversification of red-lineage phytoplankton is an important driver of divergent life history strategies among the heterotrophic bacterioplankton taxa that dominate the present-day ocean.One-half of global primary production occurs in the oceans, and more than half of this is processed by heterotrophic bacterioplankton through the marine microbial food web.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Sciences, University of Georgia, Athens, Georgia, USA.

ABSTRACT

Unlabelled: Marine bacteria in the Roseobacter and SAR11 lineages successfully exploit the ocean habitat, together accounting for ~40% of bacteria in surface waters, yet have divergent life histories that exemplify patch-adapted versus free-living ecological roles. Here, we use a phylogenetic birth-and-death model to understand how genome content supporting different life history strategies evolved in these related alphaproteobacterial taxa, showing that the streamlined genomes of free-living SAR11 were gradually downsized from a common ancestral genome only slightly larger than the extant members (~2,000 genes), while the larger and variably sized genomes of roseobacters evolved along dynamic pathways from a sizeable common ancestor (~8,000 genes). Genome changes in the SAR11 lineage occurred gradually over ~800 million years, whereas Roseobacter genomes underwent more substantial modifications, including major periods of expansion, over ~260 million years. The timing of the first Roseobacter genome expansion was coincident with the predicted radiation of modern marine eukaryotic phytoplankton of sufficient size to create nutrient-enriched microzones and is consistent with present-day ecological associations between these microbial groups. We suggest that diversification of red-lineage phytoplankton is an important driver of divergent life history strategies among the heterotrophic bacterioplankton taxa that dominate the present-day ocean.

Importance: One-half of global primary production occurs in the oceans, and more than half of this is processed by heterotrophic bacterioplankton through the marine microbial food web. The diversity of life history strategies that characterize different bacterioplankton taxa is an important subject, since the locations and mechanisms whereby bacteria interact with seawater organic matter has effects on microbial growth rates, metabolic pathways, and growth efficiencies, and these in turn affect rates of carbon mineralization to the atmosphere and sequestration into the deep sea. Understanding the evolutionary origins of the ecological strategies that underlie biochemical interactions of bacteria with the ocean system, and which scale up to affect globally important biogeochemical processes, will improve understanding of how microbial diversity is maintained and enable useful predictions about microbial response in the future ocean.

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Analysis of gene loss rate (A), lateral gene transfer rate (B), and gene duplication rate (C) versus amino acid substitution rate on the Roseobacter branches of the alphaproteobacterial phylogeny constructed using P4. For the exterior Roseobacter branches, LGT rate calculations were highly variable and did not exhibit a clock-like pattern (R2 = 0.14; P = 0.02).
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fig3: Analysis of gene loss rate (A), lateral gene transfer rate (B), and gene duplication rate (C) versus amino acid substitution rate on the Roseobacter branches of the alphaproteobacterial phylogeny constructed using P4. For the exterior Roseobacter branches, LGT rate calculations were highly variable and did not exhibit a clock-like pattern (R2 = 0.14; P = 0.02).

Mentions: The phylogenetic birth-and-death model imposed on the phylogenomic trees shows a steady trend toward streamlined genomes in the SAR11 lineage, with no abrupt changes in gene family content since the common ancestor (Fig. 2A; see also Fig. S2A and C in the supplemental material). The Roseobacter lineage exhibits a more complicated evolutionary path to net genome reduction, however (Fig. 2B; see also Fig. S2B and D), with the Roseobacter ancestor experiencing an early surge in gene content (leading to the R37 node in Fig. 2B; see also Fig. S2B and D). The model suggests that this surge occurred exclusively through gain of new families rather than expansion of existing ones (see Table S1). The calculated rate of gene loss compared to the amino acid substitution rate for Roseobacter branches varies depending on the underlying phylogenetic tree reconstruction (14 deletions per amino acid substitution for P4, 5 for RAxML, 8 for PhyloBayes), but all three predict that genes were lost at a constant rate for both ancestral and exterior branches (Fig. 3A; see also Fig. S3A and D and Table S2A). For LGT, however, calculated rates are significantly lower for ancestral than for exterior branches (Fig. 3B; see Fig. S3B and E and Table S2A), with the LGT rate following a molecular clock only for the ancestral branches (averaging 0.036, 0.015, or 0.024 gene family acquisitions per amino acid substitution, depending on tree construction; R2 > 0.69 and P < 0.001 in all cases). The notable exception is the ancestral branch leading to Roseobacter node R37, showing a significantly higher LGT rate than any other ancestral branch (see Table S2B), in agreement with the significant surge of genome content on that branch predicted by the birth-and-death model (Fig. 2B; see also Fig. S2B and D) with bootstrapped genome content data sets (see Table S3). For gene duplication, calculated rates are low in the majority of Roseobacter branches (Fig. 3C; see also Fig. S3C and F) and do not follow a molecular clock (P > 0.05) (see Table S2A). The branch leading to the Arctic strain Octadecabacter arcticus 238 is an outlier (P < 0.001; see Table S2B), regardless of whether the observed expansion of insertion sequence families are included or not (see Fig. S4), suggesting that gene duplication rates may be enhanced in polar roseobacters.


Evolution of divergent life history strategies in marine alphaproteobacteria.

Luo H, Csuros M, Hughes AL, Moran MA - MBio (2013)

Analysis of gene loss rate (A), lateral gene transfer rate (B), and gene duplication rate (C) versus amino acid substitution rate on the Roseobacter branches of the alphaproteobacterial phylogeny constructed using P4. For the exterior Roseobacter branches, LGT rate calculations were highly variable and did not exhibit a clock-like pattern (R2 = 0.14; P = 0.02).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3735120&req=5

fig3: Analysis of gene loss rate (A), lateral gene transfer rate (B), and gene duplication rate (C) versus amino acid substitution rate on the Roseobacter branches of the alphaproteobacterial phylogeny constructed using P4. For the exterior Roseobacter branches, LGT rate calculations were highly variable and did not exhibit a clock-like pattern (R2 = 0.14; P = 0.02).
Mentions: The phylogenetic birth-and-death model imposed on the phylogenomic trees shows a steady trend toward streamlined genomes in the SAR11 lineage, with no abrupt changes in gene family content since the common ancestor (Fig. 2A; see also Fig. S2A and C in the supplemental material). The Roseobacter lineage exhibits a more complicated evolutionary path to net genome reduction, however (Fig. 2B; see also Fig. S2B and D), with the Roseobacter ancestor experiencing an early surge in gene content (leading to the R37 node in Fig. 2B; see also Fig. S2B and D). The model suggests that this surge occurred exclusively through gain of new families rather than expansion of existing ones (see Table S1). The calculated rate of gene loss compared to the amino acid substitution rate for Roseobacter branches varies depending on the underlying phylogenetic tree reconstruction (14 deletions per amino acid substitution for P4, 5 for RAxML, 8 for PhyloBayes), but all three predict that genes were lost at a constant rate for both ancestral and exterior branches (Fig. 3A; see also Fig. S3A and D and Table S2A). For LGT, however, calculated rates are significantly lower for ancestral than for exterior branches (Fig. 3B; see Fig. S3B and E and Table S2A), with the LGT rate following a molecular clock only for the ancestral branches (averaging 0.036, 0.015, or 0.024 gene family acquisitions per amino acid substitution, depending on tree construction; R2 > 0.69 and P < 0.001 in all cases). The notable exception is the ancestral branch leading to Roseobacter node R37, showing a significantly higher LGT rate than any other ancestral branch (see Table S2B), in agreement with the significant surge of genome content on that branch predicted by the birth-and-death model (Fig. 2B; see also Fig. S2B and D) with bootstrapped genome content data sets (see Table S3). For gene duplication, calculated rates are low in the majority of Roseobacter branches (Fig. 3C; see also Fig. S3C and F) and do not follow a molecular clock (P > 0.05) (see Table S2A). The branch leading to the Arctic strain Octadecabacter arcticus 238 is an outlier (P < 0.001; see Table S2B), regardless of whether the observed expansion of insertion sequence families are included or not (see Fig. S4), suggesting that gene duplication rates may be enhanced in polar roseobacters.

Bottom Line: The timing of the first Roseobacter genome expansion was coincident with the predicted radiation of modern marine eukaryotic phytoplankton of sufficient size to create nutrient-enriched microzones and is consistent with present-day ecological associations between these microbial groups.We suggest that diversification of red-lineage phytoplankton is an important driver of divergent life history strategies among the heterotrophic bacterioplankton taxa that dominate the present-day ocean.One-half of global primary production occurs in the oceans, and more than half of this is processed by heterotrophic bacterioplankton through the marine microbial food web.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Sciences, University of Georgia, Athens, Georgia, USA.

ABSTRACT

Unlabelled: Marine bacteria in the Roseobacter and SAR11 lineages successfully exploit the ocean habitat, together accounting for ~40% of bacteria in surface waters, yet have divergent life histories that exemplify patch-adapted versus free-living ecological roles. Here, we use a phylogenetic birth-and-death model to understand how genome content supporting different life history strategies evolved in these related alphaproteobacterial taxa, showing that the streamlined genomes of free-living SAR11 were gradually downsized from a common ancestral genome only slightly larger than the extant members (~2,000 genes), while the larger and variably sized genomes of roseobacters evolved along dynamic pathways from a sizeable common ancestor (~8,000 genes). Genome changes in the SAR11 lineage occurred gradually over ~800 million years, whereas Roseobacter genomes underwent more substantial modifications, including major periods of expansion, over ~260 million years. The timing of the first Roseobacter genome expansion was coincident with the predicted radiation of modern marine eukaryotic phytoplankton of sufficient size to create nutrient-enriched microzones and is consistent with present-day ecological associations between these microbial groups. We suggest that diversification of red-lineage phytoplankton is an important driver of divergent life history strategies among the heterotrophic bacterioplankton taxa that dominate the present-day ocean.

Importance: One-half of global primary production occurs in the oceans, and more than half of this is processed by heterotrophic bacterioplankton through the marine microbial food web. The diversity of life history strategies that characterize different bacterioplankton taxa is an important subject, since the locations and mechanisms whereby bacteria interact with seawater organic matter has effects on microbial growth rates, metabolic pathways, and growth efficiencies, and these in turn affect rates of carbon mineralization to the atmosphere and sequestration into the deep sea. Understanding the evolutionary origins of the ecological strategies that underlie biochemical interactions of bacteria with the ocean system, and which scale up to affect globally important biogeochemical processes, will improve understanding of how microbial diversity is maintained and enable useful predictions about microbial response in the future ocean.

Show MeSH