Cite this paper:
Si CHEN, Kaixuan CUI, Wenyan ZHANG, Yicong ZHAO, Tian XIAO, Hongmiao PAN, Wuchang ZHANG, Long-Fei WU. Observations on a magnetotactic bacteria-grazing ciliate in sediment from the intertidal zone of Huiquan Bay, China[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2053-2062

Observations on a magnetotactic bacteria-grazing ciliate in sediment from the intertidal zone of Huiquan Bay, China

Si CHEN1,2,3,4, Kaixuan CUI1,2,3,4, Wenyan ZHANG1,3,4,5, Yicong ZHAO1,2,3,4, Tian XIAO1,3,4,5, Hongmiao PAN1,3,4,5, Wuchang ZHANG1,3,4, Long-Fei WU5,6
1 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology(Qingdao), Qingdao 266237, China;
4 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China;
5 International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms(LIA-MagMC), CNRS-CAS, Qingdao 266071, China;
6 Aix Marseille Univ, CNRS, LCB, IM2 B, IMM, Marseille 13009, France
Abstract:
Magnetotactic bacteria (MTB) are a group of prokaryotes having the ability to orient and swim along geomagnetic field lines because they contain intracellular magnetosomes that are synthesized through a biomineralization process. Magnetosomes have recently also been found in unicellular eukaryotes, which are referred to as magnetically responsive protists (MRPs). The magnetosomes have three origins in MRPs. In this study, we characterized a MTB-grazing ciliated MRP that was magnetically collected from intertidal sediment of Huiquan Bay, Qingdao, China. Based on 18S rRNA gene sequence analysis, the ciliated MRP was tentatively identified as Uronemella parafilificum HQ. Using transmission electron microscopy, we observed that magnetosomes having 2–3 shapes were randomly distributed within this ciliate. Energydispersive X-ray spectroscopy and high-resolution transmission electron microscopy images of the magnetosomes were consistent with them being composed of magnetite. Magnetosomes having the same shape and mineral composition were also detected in MTB that occurred in the same environment as the ciliated MRP. Statistical analysis showed that the size and shape of the magnetosomes in the ciliated MRP were similar to those in MTB. The results suggest that this ciliated MRP can graze, ingest, and digest various types of MTB. It is certainly worth noting that this is the first record of MRPs in Asian aquatic sediment and suggesting they might be widely distributed. These results also support the assertion that MRPs probably contribute to the ecological cycles of iron, and expand possibilities for research into the mechanism of magnetoreception in eukaryotes.
Key words:    magnetically responsive protist|ciliate|magnetotactic bacteria|magnetosome|graze|magnetoreception   
Received: 2021-01-08   Revised: 2021-02-25
Tools
PDF (1795 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Si CHEN
Articles by Kaixuan CUI
Articles by Wenyan ZHANG
Articles by Yicong ZHAO
Articles by Tian XIAO
Articles by Hongmiao PAN
Articles by Wuchang ZHANG
Articles by Long-Fei WU
References:
Amor M, Mathon F P, Monteil C L, Busigny V, Lefèvre C T. 2020. Iron-biomineralizing organelle in magnetotactic bacteria:function, synthesis and preservation in ancient rock samples. Environmental Microbiology, 22(9):3611-3632, https://doi.org/10.1111/1462-2920.15098.
Bazylinski D A, Schlezinger D R, Howes B H, Frankel R B, Epstein S S. 2000. Occurrence and distribution of diverse populations of magnetic protists in a chemically stratified coastal salt pond. Chemical Geology, 169(3-4):319-328, https://doi.org/10.1016/S0009-2541(00)00211-4.
Bernard C, Rassoulzadegan F. 1990. Bacteria or microflagellates as a major food source for marine ciliates:possible implications for the microzooplankton. Marine Ecology Progress Series, 64:147-155, https://doi.org/10.3354/meps064147.
Blakemore R. 1975. Magnetotactic bacteria. Science, 190(4212):377-379, https://doi.org/10.1126/science.170679.
Dieudonné A, Pignol D, Prévéral S. 2019. Magnetosomes:biogenic iron nanoparticles produced by environmental bacteria. Applied Microbiology and Biotechnology, 103(9):3637-3649, https://doi.org/10.1007/s00253-019-09728-9.
Dolan J R, Karel Š. 1997. Processing of ingested matter in Strombidium sulcatum, a marine ciliate (Oligotrichida). Limnology and Oceanography, 42(2):393-397, https://doi.org/10.4319/lo.1997.42.2.0393.
Frankel R B, Blakemore R P, Wolfe R S. 1979. Magnetite in freshwater magnetotactic bacteria. Science, 203(4387):1355-1356, https://doi.org/10.1126/science.203.4387.1355.
Gong J, Choi J K, Roberts D M, Kim S Y, Min G S. 2007. Morphological descriptions of new and little-known benthic ciliates from Ganghwa tidal flat, Korea. The Journal of Eukaryotic Microbiology, 54(3):306-316, https://doi.org/10.1111/j.1550-7408.2007.00268.x.
Leão P, Le Nagard L, Yuan H, Cypriano J, Da Silva-Neto I, Bazylinski D A, Acosta-Avalos D, de Barros H L, Hitchcock A P, Lins U, Abreu F. 2020. Magnetosome magnetite biomineralization in a flagellated protist:evidence for an early evolutionary origin for magnetoreception in eukaryotes. Environmental Microbiology, 22(4):1495-1506, https://doi.org/10.1111/1462-2920.14711.
Lefèvre C T, Trubitsyn D, Abreu F, Kolinko S, de Almeida L G P, de Vasconcelos A T R, Lins U, Schüler D, Ginet N, Pignol D, Bazylinski D A. 2013. Monophyletic origin of magnetotaxis and the first magnetosomes. Environmental Microbiology, 15(8):2267-2274, https://doi.org/10.1111/1462-2920.12097.
Mann S, Sparks N H, Walker M M, Kirschvink J L. 1988. Ultrastructure, morphology and organization of biogenic magnetite from sockeye salmon, Oncorhynchus nerka:implications for magnetoreception. Journal of Experimental Biology, 140:35-49, https://doi.org/10.1242/jeb.140.1.35.
Martins J L, Silveira T S, Abreu F, Silva K T, da Silva-Neto I D, Lins U. 2007. Grazing protozoa and magnetosome dissolution in magnetotactic bacteria. Environmental Microbiology, 9(11):2775-2781, https://doi.org/10.1111/j.1462-2920.2007.01389.x.
Medlin L, Elwood H J, Stickel S, Sogin M L. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71(2):491-499, https://doi.org/10.1016/0378-1119(88)90066-2.
Monteil C L, Lefèvre C T. 2020. Magnetoreception in microorganisms. Trends in Microbiology, 28(4):266-275, https://doi.org/10.1016/j.tim.2019.10.012.
Monteil C L, Menguy N, Prévéral S, Warren A, Pignol D, Lefèvre C T. 2018. Accumulation and dissolution of magnetite crystals in a magnetically responsive ciliate. Applied and Environmental Microbiology, 84(8):e02865-17, https://doi.org/10.1128/AEM.02865-17.
Monteil C L, Vallenet D, Menguy N, Benzerara K, Barbe V, Fouteau S, Cruaud C, Floriani M, Viollier E, Adryanczyk G, Leonhardt N, Faivre D, Pignol D, López-García P, Weld R J, Lefèvre C T. 2019. Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist. Nature Microbiology, 4(7):1088-1095, https://doi.org/10.1038/s41564-019-0432-7.
Pan H M, Dong Y, Teng Z J, Li J H, Zhang W Y, Xiao T, Wu L F. 2019. A species of magnetotactic deltaproteobacterium was detected at the highest abundance during an algal bloom. FEMS Microbiology Letters, 366(22):fnz253, https://doi.org/10.1093/femsle/fnz253.
Pan H M, Zhu K L, Song T, Yu-Zhang K, Lefèvre C, Xing S, Liu M, Zhao S J, Xiao T, Wu L F. 2008. Characterization of a homogeneous taxonomic group of marine magnetotactic cocci within a low tide zone in the China Sea. Environmental Microbiology, 10(5):1158-1164, https://doi.org/10.1111/j.1462-2920.2007.01532.x.
Rassoulzadegan F, Laval-Peuto M, Sheldon R W. 1988. Partitioning of the food ration of marine ciliates between pico- and nanoplankton. Hydrobiologia, 159(1):75-88, https://doi.org/10.1007/BF00007369.
Rodgers F G, Blakemore R P, Blakemore N A, Frankel R B, Bazylinski D A, Maratea D, Rodgers C. 1990. Intercellular structure in a many-celled magnetotactic prokaryote. Archives of Microbiology, 154:18-22, https://doi.org/10.1007/BF00249172.
Schüler D. 2002. The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. International Microbiology, 5(4):209-214, https://doi.org/10.1007/s10123-002-0086-8.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6:molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12):2725-2729, https://doi.org/10.1093/molbev/mst197.
Torres de Araujo F F, Pires M A, Frankel R B, Bicudo C E M. 1986. Magnetite and magnetotaxis in algae. Biophys. J., 50:375-378, https://doi.org/10.1016/S0006-3495(86)83471-3.
Wang R, Song W, Yi Z Z, Al-Rasheid K A S, Hu X Z. 2018. Morphology and molecular phylogeny of two new species of Spirostrombidium (Ciliophora, Oligotrichia), with a key to the species of Spirostrombidium. Systematics and Biodiversity, 16(8):743-756, https://doi.org/10.1080/147 72000.2018.1484393.
Xing S E, Pan H M, Zhu K L, Xiao T, Wu L F. 2008. Diversity of marine magnetotactic bacteria in the Huiquan bay near Qingdao city. Chinese High Technology Letters, 18(3):312-317, https://doi.org/10.3772/j.issn.1002-0470.2008.03.017. (in Chinese with English abstract)
Zhang R, Chen Y R, Du H J, Zhang W Y, Pan H M, Xiao T, Wu L F. 2014. Characterization and phylogenetic identification of a species of spherical multicellular magnetotactic prokaryotes that produces both magnetite and greigite crystals. Research in Microbiology, 165(7):481-489, https://doi.org/10.1016/j.resmic.2014.07.012.
Copyright © Haiyang Xuebao