Trophic Specialization Results in Genomic Reduction in Free-Living Marine <italic toggle="yes">Idiomarina</italic> Bacteria

ABSTRACT The streamlining hypothesis is generally used to explain the genomic reduction events related to the small genome size of free-living bacteria like marine bacteria SAR11. However, our current understanding of the correlation between bacterial genome size and environmental adaptation relies...

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Main Authors: Qi-Long Qin, Yi Li, Lin-Lin Sun, Zhi-Bin Wang, Shi Wang, Xiu-Lan Chen, Aharon Oren, Yu-Zhong Zhang
Format: Article
Language:English
Published: American Society for Microbiology 2019-02-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mBio.02545-18
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author Qi-Long Qin
Yi Li
Lin-Lin Sun
Zhi-Bin Wang
Shi Wang
Xiu-Lan Chen
Aharon Oren
Yu-Zhong Zhang
author_facet Qi-Long Qin
Yi Li
Lin-Lin Sun
Zhi-Bin Wang
Shi Wang
Xiu-Lan Chen
Aharon Oren
Yu-Zhong Zhang
author_sort Qi-Long Qin
collection DOAJ
description ABSTRACT The streamlining hypothesis is generally used to explain the genomic reduction events related to the small genome size of free-living bacteria like marine bacteria SAR11. However, our current understanding of the correlation between bacterial genome size and environmental adaptation relies on too few species. It is still unclear whether there are other paths leading to genomic reduction in free-living bacteria. The genome size of marine free-living bacteria of the genus Idiomarina belonging to the order Alteromonadales (Gammaproteobacteria) is much smaller than the size of related genomes from bacteria in the same order. Comparative genomic and physiological analyses showed that the genomic reduction pattern in this genus is different from that of the classical SAR11 lineage. Genomic reduction reconstruction and substrate utilization profile showed that Idiomarina spp. lost a large number of genes related to carbohydrate utilization, and instead they specialized on using proteinaceous resources. Here we propose a new hypothesis to explain genomic reduction in this genus; we propose that trophic specialization increasing the metabolic efficiency for using one kind of substrate but reducing the substrate utilization spectrum could result in bacterial genomic reduction, which would be not uncommon in nature. This hypothesis was further tested in another free-living genus, Kangiella, which also shows dramatic genomic reduction. These findings highlight that trophic specialization is potentially an important path leading to genomic reduction in some marine free-living bacteria, which is distinct from the classical lineages like SAR11. IMPORTANCE The streamlining hypothesis is usually used to explain the genomic reduction events in free-living bacteria like SAR11. However, we find that the genomic reduction phenomenon in the bacterial genus Idiomarina is different from that in SAR11. Therefore, we propose a new hypothesis to explain genomic reduction in this genus based on trophic specialization that could result in genomic reduction, which would be not uncommon in nature. Not only can the trophic specialization hypothesis explain the genomic reduction in the genus Idiomarina, but it also sheds new light on our understanding of the genomic reduction processes in other free-living bacterial lineages.
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spelling doaj.art-0b586bc4f0b34a669f271cdaea0611b52022-12-21T19:53:17ZengAmerican Society for MicrobiologymBio2150-75112019-02-0110110.1128/mBio.02545-18Trophic Specialization Results in Genomic Reduction in Free-Living Marine <italic toggle="yes">Idiomarina</italic> BacteriaQi-Long Qin0Yi Li1Lin-Lin Sun2Zhi-Bin Wang3Shi Wang4Xiu-Lan Chen5Aharon Oren6Yu-Zhong Zhang7State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, ChinaState Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, ChinaState Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, ChinaState Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao, ChinaState Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, ChinaDepartment of Plant and Environmental Sciences, The Alexander Silberman Institute of Life Sciences, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem, IsraelState Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, ChinaABSTRACT The streamlining hypothesis is generally used to explain the genomic reduction events related to the small genome size of free-living bacteria like marine bacteria SAR11. However, our current understanding of the correlation between bacterial genome size and environmental adaptation relies on too few species. It is still unclear whether there are other paths leading to genomic reduction in free-living bacteria. The genome size of marine free-living bacteria of the genus Idiomarina belonging to the order Alteromonadales (Gammaproteobacteria) is much smaller than the size of related genomes from bacteria in the same order. Comparative genomic and physiological analyses showed that the genomic reduction pattern in this genus is different from that of the classical SAR11 lineage. Genomic reduction reconstruction and substrate utilization profile showed that Idiomarina spp. lost a large number of genes related to carbohydrate utilization, and instead they specialized on using proteinaceous resources. Here we propose a new hypothesis to explain genomic reduction in this genus; we propose that trophic specialization increasing the metabolic efficiency for using one kind of substrate but reducing the substrate utilization spectrum could result in bacterial genomic reduction, which would be not uncommon in nature. This hypothesis was further tested in another free-living genus, Kangiella, which also shows dramatic genomic reduction. These findings highlight that trophic specialization is potentially an important path leading to genomic reduction in some marine free-living bacteria, which is distinct from the classical lineages like SAR11. IMPORTANCE The streamlining hypothesis is usually used to explain the genomic reduction events in free-living bacteria like SAR11. However, we find that the genomic reduction phenomenon in the bacterial genus Idiomarina is different from that in SAR11. Therefore, we propose a new hypothesis to explain genomic reduction in this genus based on trophic specialization that could result in genomic reduction, which would be not uncommon in nature. Not only can the trophic specialization hypothesis explain the genomic reduction in the genus Idiomarina, but it also sheds new light on our understanding of the genomic reduction processes in other free-living bacterial lineages.https://journals.asm.org/doi/10.1128/mBio.02545-18genomeIdiomarinamarine bacteriatrophic specialization
spellingShingle Qi-Long Qin
Yi Li
Lin-Lin Sun
Zhi-Bin Wang
Shi Wang
Xiu-Lan Chen
Aharon Oren
Yu-Zhong Zhang
Trophic Specialization Results in Genomic Reduction in Free-Living Marine <italic toggle="yes">Idiomarina</italic> Bacteria
mBio
genome
Idiomarina
marine bacteria
trophic specialization
title Trophic Specialization Results in Genomic Reduction in Free-Living Marine <italic toggle="yes">Idiomarina</italic> Bacteria
title_full Trophic Specialization Results in Genomic Reduction in Free-Living Marine <italic toggle="yes">Idiomarina</italic> Bacteria
title_fullStr Trophic Specialization Results in Genomic Reduction in Free-Living Marine <italic toggle="yes">Idiomarina</italic> Bacteria
title_full_unstemmed Trophic Specialization Results in Genomic Reduction in Free-Living Marine <italic toggle="yes">Idiomarina</italic> Bacteria
title_short Trophic Specialization Results in Genomic Reduction in Free-Living Marine <italic toggle="yes">Idiomarina</italic> Bacteria
title_sort trophic specialization results in genomic reduction in free living marine italic toggle yes idiomarina italic bacteria
topic genome
Idiomarina
marine bacteria
trophic specialization
url https://journals.asm.org/doi/10.1128/mBio.02545-18
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