基于比较基因组学分析海洋聚球藻对铁限制的适应机制

doi:10.11978/2023036

摘要/Abstract

摘要：

铁在海水中溶解度低, 来源有限, 是全球40%海域中浮游植物的主要生长限制因子。海洋聚球藻是一种全球分布的超微型蓝藻, 也是海洋初级生产力最主要的贡献者之一。受到近岸和大洋环境中铁来源和浓度的影响, 海洋聚球藻应对铁限制的适应机制可能存在差异。本研究基于29株全基因组测序的海洋聚球藻进行了比较基因组学分析。结果表明, 海洋聚球藻具有较高的遗传多样性, 隶属于GTDB(Genome Taxonomy Database)分类法中Cyanobiaceae科的4个属, 并且这4个属与原有NCBI(National Center for Biotechnology Information)分类法中海洋聚球藻的亚群分类具有很好的对应关系。功能注释结果表明, 近岸和大洋聚球藻的特有基因数量与种类差异较大, 近岸株中参与无机离子转运和代谢的特有基因数量大于大洋株。进一步分析海洋聚球藻铁限制相关基因后发现, 近岸株在铁的吸收、稳态调节和储存方面的能力强于大洋株, 对环境变化的感知和响应能力也更强。本研究重新梳理了海洋聚球藻的进化关系和分类地位, 并系统分析了近岸和大洋聚球藻基因组及应对铁限制的适应机制差异, 为深入理解海洋聚球藻的环境适应性提供了依据。

关键词: 比较基因组学, 海洋聚球藻, 铁限制, 适应机制

Abstract:

Low solubility and limited source of iron in seawater are the main growth limiting factors for phytoplankton in 40%of the global ocean. Marine Synechococcus is a picocyanobacteria with global distribution and is one of the most important contributors to marine prime productivity. Affected by the source and concentration of iron in coastal and oceanic environments, marine Synechococcus has different adaptive mechanisms to iron limitation. In this study, we performed a comparative genomic analysis of 29 whole genome sequenced marine Synechococcus. The results showed that marine Synechococcus had high genetic diversity and belonged to four genera of Cyanobiaceae under the GTDB (Genome Taxonomy Database) taxonomy, and these four genera corresponded well to the subtype under NCBI (National Center for Biotechnology Information) taxonomy. The results of functional annotation showed that the number and types of unique genes differed between coastal and oceanic Synechococcus, and unique gene of coastal strains are more involved in inorganic ion transport and metabolism. Further analysis of iron limitation-related genes in marine Synechococcus revealed that the coastal strain had stronger abilities of iron uptake, homeostasis regulation and storage than the oceanic strains, and had a better ability to sense and respond to environmental changes. In this study, we reviewed the evolutionary relationships and taxonomic positions of marine Synechococcus using comparative genomics, and identified the differences in the genome and adaptive mechanisms of coastal and oceanic strains in response to iron limitation, to provide a basis for better understanding of the environmental adaptation of marine Synechococcus.

Key words: Comparative genomics, marine Synechococcus, iron limitation, adaptive mechanisms

穆蓉, 朱珠, 张瑞峰. 基于比较基因组学分析海洋聚球藻对铁限制的适应机制[J]. 热带海洋学报, 2023, 42(6): 89-100.

MU Rong, ZHU Zhu, ZHANG Ruifeng. Adaptive mechanisms of iron limitation on the marine Synechococcus based on comparative genomics[J]. Journal of Tropical Oceanography, 2023, 42(6): 89-100.

图/表 9

表1

图1

图2

图3

表2

本研究中29株海洋聚球藻的基因组信息"

分离地点		基因组编号	类型	基因组大小/bp	GC含量/%	完整度/%	污染度/%
大西洋马尾藻海	WH8102	GCA_000195975.1	大洋	2434428	59.4	99.46	0
	WH7803	GCA_000063505.1	大洋	2366980	60.2	99.18	0
	WH8103	GCA_001182765.1	大洋	2429688	59.5	99.73	0.27
	UW69	GCA_900474185.1	大洋	2372121	58.7	100	0
	UW140	GCA_900474295.1	大洋	2704142	57.8	99.73	0
	UW105	GCA_900473935.1	大洋	2659417	57.5	99.46	0
	UW106	GCA_900474015.1	大洋	2479535	58	99.73	0.27
	WH8109	GCA_000161795.2	大洋	2111515	60.1	99.46	0
赤道太平洋	UW179A	GCA_900473965.1	大洋	3057835	54.5	100	0.41
	MITS9508	GCA_001632165.1	大洋	2502434	56.1	100	0.27
	MITS9509	GCA_001631935.1	大洋	3087928	55.4	99.18	0.82
	MITS9504	GCA_001632105.1	大洋	3087293	55.4	99.73	1.09
东太平洋加利福尼亚海流	CC9605	GCA_000012625.1	近岸	2510659	59.2	99.73	0
	CC9311	GCA_000014585.1	近岸	2606748	52.5	99.73	0
	CC9902	GCA_000012505.1	近岸	2234828	54.2	99.46	0
中国东海	KORDI-52	GCA_000737595.1	近岸	2572069	59.1	100	0
中国东海	KORDI-49	GCA_000737575.1	近岸	2585813	61.4	99.37	0
地中海	RCC307	GCA_000063525.1	近岸	2224914	60.8	99.64	0
地中海	BL107	GCA_000153805.1	近岸	2285034	54.2	99.46	0
红海亚喀巴湾	RS9916	GCA_000153825.1	近岸	2664873	59.8	99.73	0
红海亚喀巴湾	RS9917	GCA_000153065.1	近岸	2584918	64.5	99.46	0
波多黎马格耶斯岛	PCC7002	GCA_000019485	近岸	3409935	49.2	100	0
西太平洋	KORDI-100	GCA_000737535.1	大洋	2789000	57.5	99.46	0
新英格兰大陆架	WH8020	GCA_001040845.1	近岸	2661166	53.1	99.73	0.27
伍兹霍尔沿海海水	WH8101	GCA_004209775.1	近岸	2630292	63.3	100	0.82
北大西洋潮间带	WH8016	GCA_000230675.2	近岸	2694843	54.1	99.18	0
北大西洋	WH7805	GCA_000153285.1	大洋	2627046	57.6	99.73	0
北大西洋长岛海峡	WH5701	GCA_000153045	近岸	3280236	65.4	99.18	7.84
东太平洋	CC9616	GCA_000515235.1	大洋	2645910	56.6	99.46	0.27

表2

图4

图5

图6

表3

参考文献 63

[1]	彭铭烨, 黄婷, 张晓娟, 等, 2023. 比较基因组学解析谷物醋醋醅中巴氏醋杆菌和欧洲驹形杆菌的功能差异[J]. 微生物学报, 63(2): 638-655.
	PENG MINGYE, HUANG TING, ZHANG XIAOJUAN, et al, 2023. Comparative genomics reveals the functional differences between Acetobacter pasteurianus and Komagataeibacter europaeus in vinegar pei of Zhenjiang aromatic vinegar[J]. Acta Microbiologica Sinica, 63(2): 638-655 (in Chinese with English abstract).
[2]	郑强, 贺博闻, 史文卿, 等, 2023. 海洋超微型蓝细菌聚球藻的生态学研究进展[J]. 厦门大学学报(自然科学版), 62(3): 301-313.
	ZHENG QIANG, HE BOWEN, SHI WENQING, et al, 2023. Ecological research progress on marine picocyanobacterial Synechococcus[J]. Journal of Xiamen University (Natural Science), 62(3): 301-313 (in Chinese with English abstract).
[3]	AHLGREN N A, BELISLE B S, LEE M D, 2020. Genomic mosaicism underlies the adaptation of marine Synechococcus ecotypes to distinct oceanic iron niches[J]. Environmental Microbiology, 22(5): 1801-1815. doi: 10.1111/emi.v22.5
[4]	ANDREWS S C, ROBINSON A K, RODRÍGUEZ-QUIÑONES F, 2003. Bacterial iron homeostasis[J]. FEMS Microbiology Reviews, 27(2-3): 215-237. pmid: 12829269
[5]	CASTRUITA M, ELMEGREEN L A, SHAKED Y, et al, 2007. Comparison of the kinetics of iron release from a marine (Trichodesmium erythraeum) Dps protein and mammalian ferritin in the presence and absence of ligands[J]. Journal of Inorganic Biochemistry, 101(11-12): 1686-1691. pmid: 17804072
[6]	CHADD H E, JOINT I R, MANN N H, et al, 1996. The marine picoplankter Synechococcus sp. WH 7803 exhibits an adaptive response to restricted iron availability[J]. Fems Microbiology Ecology, 21(2): 69-76. doi: 10.1111/fem.1996.21.issue-2
[7]	CHAUMEIL P-A, MUSSIG A J, HUGENHOLTZ P, et al, 2020. GTDB-Tk: A toolkit to classify genomes with the Genome Taxonomy Database[J]. Bioinformatics, 36(6): 1925-1927. doi: 10.1093/bioinformatics/btz848
[8]	CHEN MENG-YUN, TENG WEN-KAI, ZHAO LIANG, et al, 2021. Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation[J]. The ISME Journal, 15(1): 211-227. doi: 10.1038/s41396-020-00775-z
[9]	CHENG DAN, HE QINGFANG, 2020. Iron deficiency in cyanobacteria[C]. Singapore: Springer Singapore: 181-196.
[10]	COUTINHO F, TSCHOEKE D A, THOMPSON F, et al, 2016. Comparative genomics of Synechococcus and proposal of the new genus Parasynechococcus[J]. PeerJ, 4: e1522. doi: 10.7717/peerj.1522
[11]	DORÉ H, FARRANT G K, GUYET U, et al, 2020. Evolutionary mechanisms of long-term genome diversification associated with niche partitioning in marine picocyanobacteria[J]. Frontiers in Microbiology, 11: 567431. doi: 10.3389/fmicb.2020.567431
[12]	DORÉ H, LECONTE J, GUYET U, et al, 2022. Global phylogeography of marine Synechococcus in coastal areas reveals strong community shifts[J]. Msystems, 7(6): e0065622. doi: 10.1128/msystems.00656-22
[13]	DUFRESNE A, OSTROWSKI M, SCANLAN D J, et al, 2008. Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria[J]. Genome Biology, 9: R90. doi: 10.1186/gb-2008-9-5-r90
[14]	EKMAN M, SANDH G, NENNINGER A, et al, 2014. Cellular and functional specificity among ferritin-like proteins in the multicellular cyanobacterium Nostoc punctiforme[J]. Environmental Microbiology, 16(3): 829-844. doi: 10.1111/emi.2014.16.issue-3
[15]	FLOMBAUM P, GALLEGOS J L, GORDILLO R A, et al, 2013. Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus[J]. Proceedings of the National Academy of Sciences of the United States of America, 110(24): 9824-9829.
[16]	FULLER N J, MARIE D, PARTENSKY F, et al, 2003. Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea[J]. Applied and Environmental Microbiology, 69(5): 2430-2443. doi: 10.1128/AEM.69.5.2430-2443.2003
[17]	GAO FUDAN, 2020. Iron-sulfur cluster biogenesis and iron homeostasis in cyanobacteria[J]. Frontiers in Microbiology, 11: 165. doi: 10.3389/fmicb.2020.00165 pmid: 32184761
[18]	HOPKINSON B M, BARBEAU K A, 2012. Iron transporters in marine prokaryotic genomes and metagenomes[J]. Environmental Microbiology, 14(1): 114-128. doi: 10.1111/j.1462-2920.2011.02539.x pmid: 21883791
[19]	HOPKINSON B M, MOREL F M M, 2009. The role of siderophores in iron acquisition by photosynthetic marine microorganisms[J]. Biometals, 22(4): 659-669. doi: 10.1007/s10534-009-9235-2 pmid: 19343508
[20]	JIANG HAI-BO, LU XIAO-HUI, DENG BIN, et al, 2020. Adaptive mechanisms of the model photosynthetic organisms, cyanobacteria, to iron deficiency[C]. Singapore: Springer Singapore: 197-244.
[21]	KALYAANAMOORTHY S, MINH BUIQUANG, WONG T K F, et al, 2017. ModelFinder: Fast model selection for accurate phylogenetic estimates[J]. Nature Methods, 14(6): 587-589. doi: 10.1038/nmeth.4285 pmid: 28481363
[22]	KARCAGI I, DRASKOVITS G, UMENHOFFER K, et al, 2016. Indispensability of horizontally transferred genes and its impact on bacterial genome streamlining[J]. Molecular biology and evolution, 33(5): 1257-1269. doi: 10.1093/molbev/msw009 pmid: 26769030
[23]	KATOH H, HAGINO N, GROSSMAN A R, et al, 2001. Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803[J]. Journal of Bacteriology, 183(9): 2779-2784. doi: 10.1128/JB.183.9.2779-2784.2001
[24]	KOWATA H, TOCHIGI S, TAKAHASHI H, et al, 2017. Outer membrane permeability of cyanobacterium Synechocystis sp. Strain PCC 6803: Studies of passive diffusion of small organic nutrients reveal the absence of classical porins and intrinsically low permeability[J]. Journal of Bacteriology, 199(19): e00371.
[25]	LEE M D, 2019. GToTree: A user-friendly workflow for phylogenomics[J]. Bioinformatics, 35(20): 4162-4164. doi: 10.1093/bioinformatics/btz188 pmid: 30865266
[26]	LIS H, KRANZLER C, KEREN N, et al, 2015. A comparative study of iron uptake rates and mechanisms amongst marine and fresh water cyanobacteria: Prevalence of reductive iron uptake[J]. Life, 5(1): 841-860. doi: 10.3390/life5010841
[27]	LIU XUEWU, MILLERO F J, 2002. The solubility of iron in seawater[J]. Marine Chemistry, 77(1): 43-54. doi: 10.1016/S0304-4203(01)00074-3
[28]	LÓPEZ-GOMOLLÓN S, HERNÁNDEZ J A, PELLICER S, et al, 2007. Cross-talk between iron and nitrogen regulatory networks in Anabaena (Nostoc) sp. PCC 7120: Identification of overlapping genes in FurA and NtcA regulons[J]. Journal of Molecular Biology, 374(1): 267-281. doi: 10.1016/j.jmb.2007.09.010
[29]	LUDWIG M, CHUA T T, CHEW C Y, et al, 2015. Fur-type transcriptional repressors and metal homeostasis in the cyanobacterium Synechococcus sp. PCC 7002[J]. Frontiers in Microbiology, 6: 1217.
[30]	MACKEY K R M, POST A F, MCILVIN M R, et al, 2015. Divergent responses of Atlantic coastal and oceanic Synechococcus to iron limitation[J]. Proceedings of the National Academy of Sciences of the United States of America, 112(32): 9944-9949.
[31]	MARCHETTI A, MALDONADO M T, 2016. Iron[C]. Cham: Springer International Publishing: 233-279.
[32]	MEDINI D, DONATI C, TETTELIN H, et al, 2005. The microbial pan-genome[J]. Current Opinion in Genetics & Development, 15(6): 589-594.
[33]	MIETHKE M, MARAHIEL M A, 2007. Siderophore-based iron acquisition and pathogen control[J]. Microbiology and Molecular Biology Reviews, 71(3): 413-451. doi: 10.1128/MMBR.00012-07 pmid: 17804665
[34]	MOORE J K, DONEY S C, GLOVER D M, et al, 2001. Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean[J]. Deep Sea Research Part Ⅱ: Topical Studies in Oceanography, 49(1-3): 463-507.
[35]	MOREL F M M, KUSTKA A B, SHAKED Y, 2008. The role of unchelated Fe in the iron nutrition of phytoplankton[J]. Limnology and Oceanography, 53(1): 400-404. doi: 10.4319/lo.2008.53.1.0400
[36]	MOREL F M M, PRICE N M, 2003. The biogeochemical cycles of trace metals in the oceans[J]. Science, 300(5621): 944-947. pmid: 12738853
[37]	MORRISSEY J, BOWLER C, 2012. Iron utilization in marine cyanobacteria and eukaryotic algae[J]. Frontiers in Microbiology, 3: 43. doi: 10.3389/fmicb.2012.00043 pmid: 22408637
[38]	NGUYEN L-T, SCHMIDT H A, VON HAESELER A, et al, 2015. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies[J]. Molecular Biology and Evolution, 32(1): 268-274. doi: 10.1093/molbev/msu300
[39]	PAGE A J, CUMMINS C A, HUNT M, et al, 2015. Roary: Rapid large-scale prokaryote pan genome analysis[J]. Bioinformatics, 31(22): 3691-3693. doi: 10.1093/bioinformatics/btv421 pmid: 26198102
[40]	PALENIK B, REN QINGHU, DUPONT C L, et al, 2006. Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment[J]. Proceedings of the National Academy of Sciences of the United States of America, 103(36): 13555-13559.
[41]	PARKS D H, CHUVOCHINA M, RINKE C, et al, 2022. GTDB: An ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy[J]. Nucleic Acids Research, 50(D1): D785-D794. doi: 10.1093/nar/gkab776
[42]	PARKS D H, CHUVOCHINA M, WAITE D W, et al, 2018. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life[J]. Nature Biotechnology, 36: 996-1004. doi: 10.1038/nbt.4229 pmid: 30148503
[43]	PARKS D H, IMELFORT M, SKENNERTON C T, et al, 2015. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes[J]. Genome Res, 25(7): 1043-1055. doi: 10.1101/gr.186072.114 pmid: 25977477
[44]	PITTERA J, HUMILY F, THOREL M, et al, 2014. Connecting thermal physiology and latitudinal niche partitioning in marine Synechococcus[J]. The ISME Journal, 8(6): 1221-1236. doi: 10.1038/ismej.2013.228
[45]	QIU GUO-WEI, KOEDOODER C, QIU BAO-SHENG, et al, 2022. Iron transport in cyanobacteria - from molecules to communities[J]. Trends in Microbiology, 30(3): 229-240. doi: 10.1016/j.tim.2021.06.001
[46]	QIU GUO-WEI, JIANG HAI-BO, LIS H, et al, 2021. A unique porin meditates iron-selective transport through cyanobacterial outer membranes[J]. Environmental Microbiology, 23(1): 376-390. doi: 10.1111/emi.v23.1
[47]	RAVEN J A, EVANS M C W, KORB R E, 1999. The role of trace metals in photosynthetic electron transport in O₂-evolving organisms[J]. Photosynthesis Research, 60: 111-150. doi: 10.1023/A:1006282714942
[48]	RIVERS A R, JAKUBA R W, WEBB E A, 2009. Iron stress genes in marine Synechococcus and the development of a flow cytometric iron stress assay[J]. Environmental Microbiology, 11(2): 382-396. doi: 10.1111/emi.2009.11.issue-2
[49]	ROCAP G, DISTEL D L, WATERBURY J B, et al, 2002. Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences[J]. Applied and Environmental Microbiology, 68(3): 1180-1191. doi: 10.1128/AEM.68.3.1180-1191.2002
[50]	SALAZAR V W, TSCHOEKE D A, SWINGS J, et al, 2020. A new genomic taxonomy system for the Synechococcus collective[J]. Environmental Microbiology, 22(11): 4557-4570. doi: 10.1111/emi.v22.11
[51]	SAMPERIO-RAMOS G, SANTANA-CASIANO J M, GONZÁLEZ-DÁVILA M, 2018. Variability in the production of organic ligands, by Synechococcus PCC 7002, under different iron scenarios[J]. Journal of Oceanography, 74: 277-286. doi: 10.1007/s10872-017-0457-6
[52]	SCANLAN D J, 2003. Physiological diversity and niche adaptation in marine Synechococcus[C]. Advances in Microbial Physiology, 47: 1-64.
[53]	SCANLAN D J, OSTROWSKI M, MAZARD S, et al, 2009. Ecological genomics of marine picocyanobacteria[J]. Microbiology and molecular biology reviews, 73(2): 249-299. doi: 10.1128/MMBR.00035-08 pmid: 19487728
[54]	SUNDA W G, HUNTSMAN S A, 1995. Iron uptake and growth limitation in oceanic and coastal phytoplankton[J]. Marine Chemistry, 50(1-4): 189-206. doi: 10.1016/0304-4203(95)00035-P
[55]	SUNDA W G, HUNTSMAN S A, 2015. High iron requirement for growth, photosynthesis, and low-light acclimation in the coastal cyanobacterium Synechococcus bacillaris[J]. Frontiers in Microbiology, 6: 561.
[56]	TAGLIABUE A, BOWIE A R, BOYD P W, et al, 2017. The integral role of iron in ocean biogeochemistry[J]. Nature, 543(7643): 51-59. doi: 10.1038/nature21058
[57]	TEOH F, SHAH B, OSTROWSKI M, et al, 2020. Comparative membrane proteomics reveal contrasting adaptation strategies for coastal and oceanic marine Synechococcus cyanobacteria[J]. Environmental Microbiology, 22(5): 1816-1828. doi: 10.1111/1462-2920.14876 pmid: 31769166
[58]	VERGALLI J, BODRENKO I V, MASI M, et al, 2020. Porins and small-molecule translocation across the outer membrane of Gram-negative bacteria[J]. Nature Reviews Microbiology, 18(3): 164-176. doi: 10.1038/s41579-019-0294-2 pmid: 31792365
[59]	WEBB E A, MOFFETT J W, WATERBURY J B, 2001. Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp. ): Identification of the IdiA protein[J]. Applied and Environmental Microbiology, 67(12): 5444-5452. doi: 10.1128/AEM.67.12.5444-5452.2001
[60]	WELLS M L, 1999. Manipulating iron availability in nearshore waters[J]. Limnology and Oceanography, 44(4): 1002-1008. doi: 10.4319/lo.1999.44.4.1002
[61]	WITTMERS F, NEEDHAM D M, HEHENBERGER E, et al, 2022. Genomes from uncultivated pelagiphages reveal multiple phylogenetic clades exhibiting extensive auxiliary metabolic genes and cross-family multigene transfers[J]. mSystems, 7(5): e0152221. doi: 10.1128/msystems.01522-21
[62]	XIA XIAOMIN, LEE P, CHEUNG SHUYAN, et al, 2020. Discovery of euryhaline phycoerythrobilin-containing Synechococcus and its mechanisms for adaptation to estuarine environments[J]. mSystems, 5(6): e00842-20.
[63]	XIA XIAOMIN, LIU HONGBIN, CHOI D, et al, 2018. Variation of Synechococcus pigment genetic diversity along two turbidity gradients in the China seas[J]. Microbial Ecology, 75(1): 10-21. doi: 10.1007/s00248-017-1021-z

基因分类		基因	基因描述	KEGG 编号
铁吸收	铁载体相关基因	TonB sidero	TonB dependent receptor	K02014
	孔蛋白基因	Porin	Outer membrane protein insertion porin family	K07277
	Fe³⁺转运基因	idiA/FutA	Iron deﬁciency induced protein A / iron(Ⅲ) transport system substrate-binding protein	K02012
		idiB/FutB	ABC-type Fe³⁺transport system permease component / iron(Ⅲ) transport system permease protein	K02011
		idiC/FutC	ATP binding component / iron(Ⅲ) transport system ATP-binding protein	K02010
	二价金属转运基因	NRAMP	Natural resistance associated macrophage protein, Nramp	K03322
		FTR1	FTR1 family iron permease	K07243
		ZIP	ZRT / IRT-like Protein	K14709
	Fe²⁺转运基因	FeoA	Ferrous iron transport protein A	K04758
	Fe²⁺转运基因	FeoB	Ferrous iron transport protein B	K04759
铁稳态	—	Fur	Ferric uptake regulator	K03711
		FecR	Periplasmic ferric-dicitrate binding protein FerR	K07165
		CRP	Cyclic AMP receptor protein	K10914
铁储存	铁储存蛋白	Dps	DNA-binding stress protein	K04047
		Bfr	Bacterioferritin	K03594
		Ftn	Ferritins	K02217

	相关基因/蛋白	海洋聚球藻
	相关基因/蛋白	近岸株	大洋株
铁吸收	铁载体	合成和利用铁载体的能力较强	合成和利用铁载体的能力较弱
	孔蛋白	存在	存在
	Fe(Ⅲ)转运蛋白	存在, 基因表达量相对较低	存在, 基因表达量相对较高
	Fe(Ⅱ)特异性转运蛋白	普遍存在	除生态型CRD1中不存在
铁稳态	Fur家族(FurA、Zur、PerR)	存在, 具有更复杂的调节能力	存在
	FecR	存在	仅在生态型CRD1中广泛分布
	CRP	存在	存在
铁储存	Ftn	拷贝数较多	仅在生态型CRD1中拥有多拷贝数
	Bfr	存在	不存在
	Dps	存在	存在