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Diversity of Protease-Producing Bacteria in the Bohai Bay Sediment

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Diversity of Protease-Producing Bacteria in the Bohai Bay Sediment Acta Oceanol. Sin., 2020, Vol. 39, No. 8, P. 1–11 https://doi.org/10.1007/s13131-020-1589-x http://www.hyxb.org.cn E-mail: [email protected] Diversity of protease-producing bacteria in the Bohai Bay 701.5 sediment and their extracellular enzymatic properties 684.5 1, 4† 1† 2 2 3 1 Zhenpeng Zhang , Chaoya Wu , Shuai Shao , Wei Liu , En-Tao Wang , Yan Li * 668.6 1 Key Laboratory of Coastal Biology and Utilization, Yantai Institute of Coastal Zone Research, Chinese Academy of 656.2 Sciences, Yantai 264003, China 646.2 2 Life Science College, Yantai University, Yantai 264005, China 634.0 3 Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico 621.8 City D.F. 11340, México 611.8 4 University of Chinese Academy of Sciences (UCAS), Beijing 100049, China 599.7 Received 2 May 2019; accepted 24 June 2019 584.6 © Chinese Society for Oceanography and Springer-Verlag GmbH Germany, part of Springer Nature 2020 565.1 Abstract 547.6 Protease-producing bacteria play key roles in the degradation of organic nitrogen materials in marine sediments.535.5 However, their diversity, production of proteases and other extracellular enzymes, even in situ ecological525.6 functions remain largely unknown. In this study, we investigated the diversity of cultivable extracellular protease-515.7 producing bacteria in the sediments of the Bohai Bay. A total of 109 bacterial isolates were obtained from the505.8 4 sediments of 7 stations. The abundance of cultivable protease-producing bacteria was about 10 CFU/g 495.9of sediment in all the samples. Phylogenetic analysis based on 16S rRNA gene sequences classified all the isolates486.0 into 14 genera from phyla Proteobacteria, Firmicutes, Bacteroidetes and Actinobacteria, with Pseudoalteromonas476.1 (63/109, 57.8%), Bacillus (9/109, 8.2%), Sulfitobacter (8/109, 7.3%) and Salegentibacter (6/109, 5.5%) as the466.2 dominant taxa. Enzymatic inhibition tests indicated that all the tested isolates produced serine and/or456.3 metalloprotease, with only a small proportion producing cysteine and/or aspartic proteases. Several extracellular446.4 enzyme activities, including alginase, lipase, amylase and cellulose, and nitrate reduction were also detected for436.5 strains with higher protease activities. According the results, the protease-producing bacteria could also be426.6 participate in many biogeochemical processes in marine sediments. Our study broadened understanding and416.7 knowledge on the potential ecological functions of protease-producing bacteria in marine sediments. 406.8 Key words: protease-producing bacteria, diversity, inhibition test, multi-extracellular enzymes 393.2 Citation: Zhang Zhenpeng, Wu Chaoya, Shao Shuai, Liu Wei, Wang En-Tao, Li Yan. 2020. Diversity of protease-producing bacteria in the378.0 Bohai Bay sediment and their extracellular enzymatic properties. Acta Oceanologica Sinica, 39(8): 1–11, doi: 10.1007/s13131-020-1589-x 368.1 344.0 1 Introduction 311.9 pecially in the sediment ecosystems. However, the diversity of311.7 Polymeric and particulate organic matters carry abundant or-300.8 these bacteria and their extracellular enzymes remain largely un-300.4 ganic nitrogen (OrgN), which are considered the main nitrogen289.6 known. 289.1 sources in marine sediment environments (Thamdrup and Dals-278.5 Protease producing bacteria are widely spread in marine sed-278.1 gaard, 2008). In the nitrogen cycle, the OrgN are usually decom-267.4 iments. For example, 30 out of the 98 strains isolated from South-267.0 posed into dissolved OrgN, followed by a series of ammonifica-256.3 ern Okinawa Trough possessed protease-producing abilities, dis-255.9 tion, nitrification and denitrification processes that are carried245.1 tributed in the genera Bacillus, Cobetia, Halomonas, Pseudomo-244.8 out by marine microorganisms (Hunter et al., 2006; Thamdrup234.0 nas, Psychrobacter, Myroides, Planococcus, Sporosarcina and233.7 and Dalsgaard, 2008). Proteins are the main building blocks of222.9 Wangia (Dang et al., 2009). By using selective media, diverse pro-222.6 organismal tissues, and protease producing bacteria are known211.8 tease producing bacteria were isolated from the sub-Antarctic211.5 as the main degraders of organic nitrogen in the marine environ-200.6 sediment (Olivera et al., 2007), the deep South China Sea sedi-200.4 ment (Zhang et al., 2015; Zhou et al., 2009). These bacterial189.5 ment (Zhou et al., 2009), coastal sediments of King George Is-189.3 groups secrete extracellular proteases that degrade proteins into178.4 land, Antractica (Zhou et al., 2013), enclosed the Jiaozhou Bay178.3 peptides and amino acids, which can be easily taken up by other167.3 (Zhang et al., 2015) and the Laizhou Bay (Li et al., 2017). In these167.2 bacteria for subsequent metabolism and processing (Zhao et al.,156.1 studies, the protease producing bacteria were classified under156.1 online145.0 first 145.0 2012). Therefore, protease-producing bacteria play important the genera Alcanivorax, Alteromonas, Burkholderia, Caulobacter, roles in the biogeochemical cycles of marine environments, es-133.9 Celeribacter, Halomonas, Hyphomonas, Idiomarina, Marinobac-131.8133.9133.8 129.5 Foundation item: The National Natural Science Foundation of China under contract Nos 31600009 and 31800099; the Key Research118.3 and Development Program of Hebei Province under contract No. 19273802D; the STS Program of Chinese Academy of Sciences and107.3 Fujian Province under contract No. 2017T3019; the Yantai Science and Technology Project under contract No. 2018ZHGY074; the96.3 Joint Fund of Jilin Province and Chinese Academy of Sciences for High-tech Industrialization under contract No. 2019SYHZ0036; En-85.3 Tao Wang was supported by the projects under contract Nos SIP 20150597 and 20160883 authorized by IPN, Mexico. 74.3 *Corresponding author, E-mail: [email protected] 63.3 † These authors contributed equally to this work. 52.3 48.0 291.5 540.0 55.0 303.5 2 Zhang Zhenpeng et al. Acta Oceanol. Sin., 2020, Vol. 39, No. 8, P. 1–11 ter, Microbulbifer, Photobacterium, Pseudoalteromonas, Pseudo-730.0 being dumped into it resulted to it becoming the most heavily ex-730.0 monas, Psychrobacter, Rheinheimera, Ruegeria, Shewanella,719.1 ploited and polluted marine areas in China. Therefore, the de-719.2 Sphingopyxis, Sulfitobacter and Vibrio of the phylum Proteobac-708.3 terioration of water quality accompanied by algal blooms, have708.4 teria; Bacillus, Exiguobacterium, Halobacillus, Jeotgalibacillus,697.4 occurred as manifestations of severe environmental problems in697.7 Oceanobacillus and Planococcus of Firmicutes; Aequorivita, Asin-686.6 this sea (Feng et al., 2011; Hu et al., 2010; Mu et al., 2017). With686.9 ibacterium, Flavobacterium, Formosa, Gillisia, Lacinutrix,675.7 the increasing problems on water pollution, the microbial com-676.1 Psychroserpens, Salegentibacter, Olleya and Zobellia of Bacteroid-664.9 munity in this aquatic ecosystem, especially the bacteria have665.4 etes; Arthrobacter, Janibacter, Leifsonia, Microbacterium, Micro-654.0 abilities to degrade organic materials, such as protein, alginate654.6 coccus, Nocardioides, Nocardiopsis and Streptomyces of Actin-643.2 and some pollutant chemical compound, are also expected to643.9 obacteria, dominated by Alteromonas, Bacillus, Flavobacterium,632.3 vary. However, the diversity of protease-producing bacteria in633.1 Lacinutrix, Photobacterium, Pseudoalteromonas and Vibrio. And621.5 this ecosystem and the characteristics of the proteases they pro-622.3 analyses of hydrolytic abilities towards different protein sub-610.6 duce remain little understood. Understanding of the proteases611.6 strates and inhibition tests indicated that all of these bacteria599.8 and other extracellular enzymes produced by these bacteria600.8 could decompose casein and/or gelatin and produce serine588.9 could not only facilitate the exploration of the other novel en-590.1 and/or metalloproteases (Li et al., 2017; Olivera et al., 2007;578.1 zyme-producing bacteria for biotechnological or industrial ap-579.3 Zhang et al., 2015; Zhou et al., 2009, 2013). 567.2 plications but would also help elucidate in situ biogeochemical568.5 Although the culture independent approaches has been ap-556.4 processes mediated by these microorganisms. Aiming to uncov-557.8 plied to detecting microbial resource reserves including the un-545.5 er the diversity of cultivable protease-producing bacterial com-547.0 cultivable taxa, isolation remains a necessary approach to obtain534.7 munity in the Bohai Bay, we isolated the proteolytic bacteria and536.3 novel microbes especially for screening specific functional isol-523.8 characterized their extracellular proteases using hydrolytic activ-525.5 ates with biotechnological application potentials (He et al., 2016;513.0 ity towards different protein substrates. We also tested factors514.7 Sfanos et al., 2005). For example, recent studies on protease-pro-502.1 that could inhibit their activity. Lastly, several other extracellular504.0 ducing bacteria using culturing method still obtained new groups491.3 enzymes production and nitrate reduction abilities were also493.2 482.5 of bacteria possessing higher protease producing abilities than480.4 tested. previous studies (Li et al., 2017). 469.6 The Bohai Bay, located in the northern coast of China, covers458.8 2 Materials and methods 460.4 2 a total area of 14 700 km , corresponding to 20% of the total area448.1 of the Bohai Sea. It is the largest semi-enclosed shallow water437.3 2.1 Ocean sediment collection and physicochemical character de-438.3 basin in the western region of the Bohai Sea. It is an important426.6 termination 427.3 spawning and traditional fishing grounds, and an aquaculture415.9 A total of 7 sediment samples were collected from the Bohai416.4 zone for economically important fish, shrimp and crab species405.1 Bay (GPS: 38.35°–39.07°N and 117.95°–118.95°E, Fig. 1 and Table 1)405.6 2 (Fu et al., 2016; Hu et al., 2010; Sun et al., 2011; Mu et al., 2017). In394.4 in April 2014 using a 0.05 m stainless steel Gray O’Hara box394.7 addition, the Bohai Bay costal area is one of the three most383.6 corner as previously described (Li et al., 2017).
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