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Abbreviation (ISO4): Prog Chem      Editor in chief: Jincai ZHAO

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Progress in Chemistry >

2024 , Vol. 36 >Issue 5: 771 - 782

DOI: https://doi.org/10.7536/PC231014

Review

Mercury Methylation in Periphyton and Its Impact on the Fate of Methylmercury in Aquatic Environments

  • Zhe Chen 1, 2, 3 ,
  • Yuping Xiang , 2, 3, 4, * ,
  • Yongguang Yin 1, 2, 3 ,
  • Yanwei Liu 2, 3 ,
  • Lufeng Chen 1 ,
  • Yong Liang 1 ,
  • Dingyong Wang 4 ,
  • Yong Cai 2, 5
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  • 1 School of Environment and Health, Jianghan University, Wuhan 430056, China
  • 2 State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
  • 3 Laboratory of Environmental Nanotechnology and Health Effect, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
  • 4 College of Resources and Environment, Southwest University, Chongqing 400715, China
  • 5 Department of Chemistry and Biochemistry, Florida International University, Miami 33199, United States
* e-mail:

Received date: 2023-10-30

  Revised date: 2024-01-22

  Online published: 2024-03-15

Supported by

National Natural Science Foundation of China(42277208)

National Natural Science Foundation of China(22006151)

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Abstract

mercury(Hg)is an important global pollutant.the aquatic environment is an important sink of mercury and the most important site for methylation and bioaccumulation.as one of the most important primary producers,periphyton is widely present in lakes,wetlands,streams,and other aquatic environments.Compared to water columns,periphyton has enhanced mercury methylation potential,which is an important source of methylmercury in aquatic environments and a key pathway for mercury entering into food chains.periphyton has diverse microbial structures and exhibits highly complex functionality.the interactions among different microorganisms result in distinct redox gradients within periphyton,forming an anoxic microenvironment conducive to mercury methylation.On the one hand,algae and bacteria in periphyton can accumulate inorganic Hg(Ⅱ)from the surrounding water,providing sufficient substrate for mercury methylation.On the other hand,periphyton is rich in metabolic secretions from various algae and bacteria,with functional groups(such As thiol groups)that can regulate the speciation of inorganic Hg(II)and enhance its bioavailability.in addition,different microorganisms can share metabolites,which can enhance the abundance and metabolic activity of Hg-methylating bacteria,thus promoting the production of methylmercury.Overall,clarifying the mercury methylation mechanism and bioaccumulation in periphyton contributes to a further understanding of the source and fate of methylmercury in aquatic environments,and provides scientific basis and data support for accurately assessing mercury pollution and environmental risks。

Contents

1 Introduction

2 Periphyton is an important site for mercury methylation in aquatic environments

2.1 Periphyton has elevated MeHg levels

2.2 Periphyton has enhanced mercury methylation potential

3 Periphyton significantly affects the fate of MeHg in aquatic environments

3.1 Periphyton is a key entrance for mercury entering into food chains

3.2 Periphyton is an important source of MeHg in water column

4 Mercury methylation in periphyton

4.1 Periphyton can accumulate Hg(Ⅱ)in aquatic environments,providing substrates for mercury methylation

4.2 Bioavailability of Hg(Ⅱ)

4.3 Activity of mercury-methylating bacteria in periphyton

5 Conclusion and outlook

Key words： mercury; methylmercury; periphyton; accumulation; methylation; food chain

Cite this article

Zhe Chen , Yuping Xiang , Yongguang Yin , Yanwei Liu , Lufeng Chen , Yong Liang , Dingyong Wang , Yong Cai . Mercury Methylation in Periphyton and Its Impact on the Fate of Methylmercury in Aquatic Environments[J]. Progress in Chemistry, 2024 , 36(5) : 771 -782 . DOI: 10.7536/PC231014

1 Introduction

Mercury(Hg)is a global pollutant with long distance transport(atmospheric residence time 0.5~1 year),high toxicity and high bioaccumulation effects[3][4]。 Mercury in nature mainly comes from natural sources,such as volcanic eruptions and forest fires,and anthropogenic sources,such as small-scale artisanal gold mining and fossil fuel burning[5]。 In 2015,mercury emissions into the atmosphere from anthropogenic sources were as high as 2220 t[5]。 in the natural environment,mercury mainly exists In the forms of elemental mercury(Hg(0)),inorganic divalent mercury(Hg(Ⅱ))and methylmercury(MeHg),and different forms can be transformed into each other[6]。 Among them,methylmercury is a strong neurotoxin,which can cause serious damage to the developing fetal brain,and can also cause kidney,heart,muscle and even genetic diseases[7]。 Consumption of contaminated aquatic products and rice is the main route of human exposure to methylmercury[8]。 Therefore,a comprehensive analysis of the sources and fate of methylmercury in the aquatic environment is the key to understanding the biogeochemical cycle of mercury and health risks。
Methylmercury in the environment mainly comes from the biotic and abiotic methylation of inorganic Hg(Ⅱ)[9][10]。 Among them,mercury methylation mediated by anaerobic microorganisms such as sulfate-reducing bacteria,iron-reducing bacteria and methanogens is the dominant pathway[11⇓~13]。 This process is mainly mediated by the hgcAB gene,which encodes the HgcA and HgcB proteins that function as reduced electron donors to the methyl carrier corrinoid protein and corrinoid protein,respectively,in the mercury methylation process[14][14]。 the formation of methylmercury is related to the composition,abundance and activity of mercury-methylating microorganisms,and is also controlled by the bioavailability of mercury in the environment[9]。
It is generally believed that sediment,anoxic water column and sediment-water interface are the main sites of methylmercury production in the aquatic environment[15][16][17][18,19]。 However,recent studies have found that the methylation of mercury in sediment and its diffusion into the water body are not sufficient to explain the high concentration of methylmercury in the water column[19]。 This suggests a possible in situ mercuric methylation process in the water column[19⇓~21]。 Recent studies have shown that the dissolved phase,suspended particulate matter,and fouling organisms in the water column are also important sites of mercury methylation[20][22,23][24]。 Among them,Periphyton(Periphyton or Periphytic biofilms)usually have a stronger ability to methylate mercury[25⇓~27]。 in some ecosystems,its methylation potential even exceeds that of sediment,which plays an extremely important role In the biogeochemical cycle of mercury[25,26]。 periphyton is an aggregate composed of periphyton,periphyton,bacteria,fungi,organic detritus,zoogloea and sediment,which mainly accumulates on the surface of aquatic plants,sediments,rocks or other solids,and is enclosed in Extra cellular polymeric substances(EPS)with high water content[28,29][30,31]。 as one of the most important primary producers in the aquatic environment,fouling organisms widely exist in lakes,wetlands,streams and other ecosystems,which can provide a living environment for a variety of microorganisms(such As mercury methylating bacteria)[28]。 A large number of studies have shown that periphyton can not only adsorb or absorb mercury from the aquatic environment,but also further convert inorganic mercury into methylmercury,which can be enriched and amplified along the food chain[2,25,32⇓⇓~35]。 in this paper,the accumulation and methylation of mercury by periphyton in different aquatic environments were summarized,and the effects of biodiversity and unique redox gradient in periphyton on the activity of mercury-methylating bacteria and the bioavailability of mercury were discussed.It is expected to provide a scientific basis for a comprehensive understanding of the biogeochemical cycle and health risks of mercury,and to provide theoretical support for the study in this area。

2 Periphyton is an important site of mercury methylation in aquatic environment

Sediment and anoxic water column are generally considered to be the most important sites of mercury methylation and sources of methylmercury in the aquatic environment[15,16]。 However,studies in the past 20 years have shown that periphyton has a very high concentration of methylmercury and a strong ability to methylate mercury.Compared with sediment and water column,periphyton shows more active mercury methylation process in a variety of aquatic environments(such as lakes,rivers and marshes).in addition,the distribution of fouling organisms in the water environment is more extensive than that of sediment,which can not only adhere to various solid substrates such as the roots of aquatic plants,rocks,wood and the surface of sediment,but also float on the surface of the water body with the attached substrates,and have a more direct impact on methylmercury in the water body[36,37]。 Therefore,fouling organisms may be a previously overlooked and more important source of MeHg in the aquatic environment。

2.1 Periphyton has a high concentration of methylmercury

Sessile organisms are widely distributed in various aquatic environments,such as lakes,streams,and wetlands.Mercury concentrations and methylation potentials of fouling organisms vary greatly in different environments(Table 1).in general,in aquatic environments such as rivers,temperate lakes,and marshes,periphyton has higher MeHg concentrations than sediment and water column[38⇓⇓~41][25][42,43]。 For example,in the Florida Everglades,although the（2.4~92 ng·g-1）of total mercury concentration in periphyton is significantly lower than the soil（9.3~350 ng·g-1）,However,its methylmercury concentration（0.052~9.4 ng·g-1）is comparable to soil（0.04~12 ng·g-1）,and even its average wet season（2 ng·g-1）is higher than soil（0.87 ng·g-1）[43]。 In the alluvial plain lake of the Beni River in the Amazon Basin,the total mercury（54~182 ng·g-1）and methylmercury（7~28.2 ng·g-1）in aquatic plants and attached organisms were higher than those in sediments(total mercury：46~79 ng·g-1,methylmercury：0.2~2.7 ng·g-1）[38]。
表1 Contents of total mercury and methylmercury in fouling organisms, water bodies and sediments in different water environments

Table 1 Mercury and methylmercury concentrations of periphyton,water,and sediment in different aquatic environments

Substrates Environments Periphyton Water Sediment Ref
THg/ng·g−1 MeHg/ng·g−1 MeHg/THg/% THg/ng·L−1 MeHg /ng·L−1 THg/ng·g−1 MeHg/ng·g−1
Rock River Idrijca 137~86100 2.48~495.50 0.18~8.76 6.45~63.10 0.03~0.10 5000~727000 3.00~10.00 41
Ludwigia peploides Sanguinet lake, Aureilhan lake 42.90~76.10a 1.00~11.40 3.00~13.00 1.00~1.50 0.40~0.50 0.10 0 25
Teflon artificial substrates Lake Croche 82.80~182 3.61 - 0.84~2.26 0~0.77 - - 49
Glass slides The Petit-Saut 116.00~161.00 32.00~64.00 27.59~39.75 0.52~2.27 0.12~1.57 - - 50
Rock River Idrijca 20.00~293000 2.17~180.00 - 0~212.00 0.01~0.29 210~6380000 0.30~19.30 40
Wood and rock Seasonal Forest Pools 46.55~188.89 2.10~16.10 1.40~24.30 3.80~22.60 0.18~1.28 - - 51
Paspalum Tapajós River 121~239 2.50~7.30 2.00~6.60 0.43~1.88 0.01~0.04 - - 39
Sediment and wood Little Wekiva River
 71.87~389.30 25~534.60 (ng·m−2) 1.95~5.12 - - - - 52
Sediment and wood Santa Fe River 3.62~12080 51.43~3798 (ng·m−2) 0.96~8.07 - - - - 52
Sediment and wood St. Marys River 57.74~749.30 35.34~218.50 (ng·m−2) 2.92~12.03 - - - - 52
Sediment and rock Beaverton Creek 308.90~739.10 13.63~2458 (ng·m−2) 0.63~2.45 - - - - 52
Sediment and rock Lookout Creek 28.60~425.90 1.33~432.30 (ng·m−2) 0.61~3.48 - - - - 52
Sediment and rock Evergreen River 117.90~510.80 35.23~3653 (ng·m−2) 6.38~13.39 - - - - 52
Sediment and rock Oak Creek 119.90~722.20 213.00~2589 (ng·m−2) 1.33~6.73 - - - - 52
Sediment and rock Pike River 92.46~261.80 14.73~1751 (ng·m−2) 3.23~7.12 - - - - 52
Teflon artificial substrates Boreal shield lake, Lake Croche 88.00~229.00 1.99~3.61 0.90~4.10 - - - - 53
Rock Boreal Shield Lakes 42.40~271.70 3.10~55.30 2.00~36.00 - - - - 54
Microscopy glass slides South Carpathian region and Danube River 54.00~262.00 - - 0.44~2.19 - - - 55
Totora High-Altitude Andean lake
reservoir		 60.60~920.70 2.90~26.50 2.40~9.50 - - - - 56
Aquatic macrophytes Beni River, Bolivian Amazonia 54.00~182.00 7~28.20 - - - 46.00~79.00 0.20~2.70 38
Paspalum. repens Tapajós river 67.00~198.00 1.00~6.00 6.90a - - - - 32
Macrophyte,floating mat, soil Everglades 2.40~92.00 0.04~9.40 - 0.91~8.30 0.04~3.80 9.30~350 0.04~12.00 43
Rock EFPC - 6.00~19.00 - 170.00~670.00b 0.05~0.65 - - 57
Frosted plexiglass Near Everglades 287.80a - - 20.00a - 96.30a - 58
Rock Streams in New Brunswick 260.00 20.00 - - - - - 59
Creek substrate Arivaca Lake 110.00~1900 10.00~300.00 - - 0.03~1.64 10.40~126.00 0.45~1.54 60
Cobbles EFPC 8000~50000b 20.00~57.00b - 50.00~730.00b 0.10~0.18b - - 61
Macrophyte Lake St. Pierre - 2.00~16.00 - - - - - 26
Rock Eastern Canadian Shield 15.00~398.00 1.00~68.00 - - - - - 62
Macrophyte Lake St. Pierre 2.00~284.00 0.10~24 - - - - - 63

“-”-Not available;a-the data is average value;b-the data is estimated from The graph in The reference

Similarly,in the Idrijca river,which was once polluted by mercury mining,although the sediment had a higher total mercury concentration(sediment：210~6380 000 ng·g-1,periphyton：20~293 000 ng·g-1）,the periphyton methyl mercury concentration（2.17~180 ng·g-1）was significantly higher than sediment（0.3~19.3 ng·g-1）.In autumn,the average concentration of MeHg in the river was as high as 180 ng·g−1,and even 100 times the concentration of MeHg in the sediment at some sampling sites[40]。 in general,many aquatic environments have high concentrations of MeHg in periphyton,especially in aquatic ecosystems such as tropical lakes。

2.2 The fouling organisms have strong ability to methylate mercury.

the fouling organisms not only have high MeHg concentrations,but also have high Hg methylation capacity(Table 2).Through in situ culture,isotope tracer and other techniques,it has been proved that fouling organisms have strong mercury methylation ability and are important mercury methylation sites in The water environment[32,44⇓~46]。
表2 Methylation ability of periphyton in different aquatic environments

Table 2 Mercury methylation potential of periphyton in different aquatic environments

Substrates Environments Methylation incubation site
（in situ or at lab）		 Methylation rate constants/d−1 Demethylation rate constants/d−1 Net MeHg production rates/% Ref
E. crassipes
roots		 Guapore River, Amazonia, Brazil At lab - - 6.20~25.60 46
Paspalum. repens Tapajós river In situ - - 0.80~22.80 32
Ludwigia peploides Sanguinet lake, Aureilhan lake, Escource river, France At lab - 3.00~7.00 25
L. helminthorrhiza,
P. densiflorum		 Beni River Basin, Bolivian Amazon At lab 0.20~36.10
(% MeHg·24h−1)		 - 0.20~4.20
(sediment: 6.37~12.60)		 45
E. crassipes roots Itaúba lakes, Zé Pedro lake, Brazil In situ - - 5.10~29.20 64
Floating mat, epiphytic periphyton Everglades At lab 0~0.02 - 2.00~5.00 (10−3) 65
Submerged macrophytes Lake St. Pierre (Quebec, Canada) In situ 15.00~18.00(10−4) 0.08~0.22 - 66
Totora Lake Titicaca At lab 0.04~0.08 - - 67
Teflon artificial
substrates		 Boreal shield lake, Lake Croche At lab 0.16~5.90
(10−4·h−1)		 - 0.04~0.74 53
Eichhornia crassipes, Polygonum densiflorum roots Lake La Granja in Bolivia At lab 17.00~165.00
( pg·g−1·12h−1)		 - - 68
Polypropylene mesh, PVC East Fork Poplar Creek (EFPC) At lab 2.15~5.23(10−5) 0.07~0.27 - 1
E. crassipes,
Myriophyllum spicatum		 Lagoinha lake At lab - - 1.60~30.20 24
Macrophytes Lake St. Pierre In situ 0~0.14 0.10~0.14 - 26

“-”-Not available

For example,a study based on Everglades in Florida,USA,found that the mercury methylation rate of fouling organisms was 17%,while that of sediment at the same site was only 10%[44]。 In rivers and lakes in southwestern France,the researchers used isotope tracer techniques to compare the mercury methylation capacity of water column,sediment and fouling organisms（199Hg(II)）.The results showed that the production rate of MeHg in fouling organisms was about 10 times higher in（3.0~7.0%·d-1）than in sediment(up to 0.9%·d-1）),while almost no MeHg was detected in water column[25]。 In Lake St.-Pierre,North America,the net MeHg yield from fouling organisms,（-126~+200 ng·m-2·d-1）,was two orders of magnitude higher than the sediment（-2.1~+5.5 ng·m-2·d-1）[47][48]。
The above studies show that in aquatic environments such as lakes,rivers and wetlands,periphyton has a strong ability to methylate mercury,even stronger than water column and sediment in some aquatic environments。

3 The fate of methylmercury in aquatic environment is significantly affected by fouling organisms.

periphyton not only has a very strong ability to methylate mercury,but also is an important source of methylmercury for the water column and aquatic organisms.On the one hand,Periphyton is an important primary producer in a variety of aquatic environments and the main source of material and energy in aquatic ecosystems,so methylmercury can enter the food chain with the ingestion of invertebrates and fish,and be transferred and amplified along the food chain,and accumulated in aquatic organisms[35,69]。 Compared with sediment,fouling organisms are more widely distributed in the aquatic environment,and the methylmercury produced by fouling organisms is more easily ingested by aquatic organisms[38]。 On the other hand,fouling organisms undergo periodic growth and decay and decomposition in the aquatic environment,so they are also an important source of methylmercury in the water column[2]。

3.1 Periphyton is an important source of methylmercury entering the food chain

as one of the most important primary producers in the aquatic environment,fouling organisms are the main food source of aquatic organisms such As fish and shrimp,and are the important basis of the aquatic food chain[38,70]。 MeHg in attached organisms can enter the food chain with the ingestion of invertebrates,and be enriched and amplified along the food chain,affecting the level of MeHg in the whole food chain(Figure 1-(8,9))[33,35,65]。
图1 水环境中附着生物的汞甲基化过程及其对水体甲基汞归趋的影响（附着生物主要通过以下途径影响水环境中的汞循环：(1) 从水体中富集Hg(Ⅱ)；(2~5) 附着生物内部藻类和非汞甲基化细菌通过影响Hg(II)的赋存形态和汞甲基化细菌的活性影响汞甲基化；(6) 甲基化细菌介导的Hg(Ⅱ)甲基化；(8, 9) 无脊椎动物及鱼类对附着生物的摄食，使汞进入食物链富集累积；(10) 附着生物向水柱释放甲基汞）（根据文献[1,2]重绘）

Fig. 1 Hg methylation in periphyton and its impact on the fate of methylmercury in aquatic environments (Periphyton affects Hg cycling in aquatic environments mainly through the following pathways: (1) Accumulation of Hg(II) from surrounding water. (2-5) Algae and non-methylators within periphyton affect Hg(II) speciation and the activity of Hg-methylating bacteria, thereby affecting Hg methylation. (6) Methylation of Hg(II) by Hg-methylating bacteria. (8, 9) Invertebrates and fish consume periphyton, leading to MeHg accumulation in food webs. And (10) release of MeHg into the water column) (modified from ref 1,2)

in lake ecosystems,algae In fouling organisms are the main contributors to primary productivity,which can account for 0.7%to 92.3%of the total algae productivity[69]。 In lake Mee,Iceland,fouling organisms contributed about 71.05%of the total primary productivity(fouling organisms+phytoplankton+macrophytes)of the Lake[71]。 The concentrations ofδ15N andδ34S in Gambusia affinis in Everglades,Florida,were significantly correlated with the fouling organisms using isotope tracer technique,suggesting that fouling organisms are an important basis of the aquatic food chain[72]。 the above studies fully show that fouling organisms are important energy sources and important hubs of material transfer in The water environment。
in addition,in many aquatic environments,fouling organisms are also the main source of methylmercury in aquatic organisms.in Everglades,Florida,Gambusia total mercury concentrations and high bioconcentration factors generally occur in areas with high concentrations of MeHg in periphyton[33]。 There was a significant positive correlation between the total mercury content and the methyl mercury content in the periphyton(R=0.465,P<0.001,N=110),suggesting that the methyl mercury in the periphyton was the main source of mercury in Gambusia affinis[43]。 the model calculation shows that 10%(1.5 kg)of the total MeHg in the fouling organisms can enter the mosquito fish population through the food chain in the wet season,up to 73%of the total Hg in the mosquito fish,which proves that the fouling organisms contribute significantly to the bioaccumulation of Hg[2]。 Methylmercury in invertebrates in Lake St.Pierre,Canada,is also mainly derived from periphyton[73]。
the transfer efficiency of methylmercury between fouling organisms and fish populations is high,which accelerates the accumulation of methylmercury in aquatic organisms.For example,in Lake La Granja,located in the Amazon Basin,the Biomagnification factor(BMF)between attached organisms and primary consumers in different seasons can range from 1 to 1.8,which is much higher than that of sediment(BMF is 0.6)[38]。 Based on the study of the East Fork Poplar river near Oak Ridge In the United States,the attached organisms have high methylmercury content and play a very important role in the enrichment of methylmercury in the River;in the food chain with periphyton as the primary producer,the biomagnification factor of methylmercury between adjacent trophic levels is as high as 3.16~31.62[61]。 Similarly,in Dongcha Baiyang River,not only the MeHg content in the fish was significantly positively correlated with that in the periphyton,but also the MeHg accumulation rate from the periphyton（1.93×10-4~4.2×10-3μg·m-2·day-1）could reach or even exceed the mercury methylation rate of the periphyton（2.58~4.30μg·m-2·day-1）（The MeHg accumulation rate/periphyton mercury methylation rate of the fish was about 4.5%-165%[57]。 Attached organisms continuously provide methylmercury to the food chain,which further increases the enrichment of methylmercury in the food chain。
in addition,compared with other food chains,the food chain based on attached organisms has stronger stability and higher accumulation of methylmercury.For example,in the case of changing hydrological conditions in alluvial plain rivers,periphyton can stably support the longest food chain compared to sediment,suspended matter,and macrophytes[38]。 After biomagnification,the methylmercury content of organisms at higher trophic levels in the food chain can reach quite high levels[38]。 The periphyton based food chain shows the highest MeHg concentrations throughout the seasonal cycle,with invertebrates containing up to 13~597 ng·g−1MeHg.In contrast,there is only one sediment-based food chain,and the methylmercury content of invertebrates in this food chain is only 1.15 ng·g-1,which is much lower than that of the attached organism food chain[38]。 the above studies show that fouling organisms play a vital role in the enrichment of methylmercury in the food chain of water bodies。

3.2 Periphyton is an important source of methylmercury in the water column

Periphyton not only affects MeHg levels in aquatic organisms through the food chain,but is also an important source of MeHg in the water column(Figure 1-(10))[2]。 Comparing the concentrations of total mercury and methylmercury in different waters,it was found that there was no significant correlation between them[74]。 It is generally believed that sediment is the main site of mercury methylation in aquatic environment.However,for deeper lakes,methylmercury produced by anoxic sediment may be fixed by sulfur-containing minerals(such as tetragonal pyrite)and difficult to release into the water column[75]。 in some reservoir environments,the content of methylmercury in bottom water is much higher than that in interface water and surface sediment interstitial water[76]。 Therefore,the methylation of mercury in sediment is difficult to explain the methylmercury in the water column.in addition,in situ methylation of mercury in water has been observed in aquatic environments such as lakes and oceans,indicating that there may be other factors controlling the level of methylmercury in the water column[21,77,78]。
Sessile organisms are widely distributed in the aquatic environment and undergo periodic growth,decline and decomposition,which are very sensitive to changes in environmental conditions(such as water level fluctuations)[79]。 Therefore,the high mercury methylation capacity of periphyton suggests that it may be the main source of methylmercury in the water column.With the increase of the distance from the periphyton,the content of methylmercury in the water body showed a decreasing trend:the periphyton pore water was the highest,followed by the overlying water,and the surface water was the lowest[2]。 the distribution trend of methylmercury is consistent with the change trend of total Dissolved organic carbon(DOC)in water,indicating that methylmercury can diffuse into the surrounding water with Dissolved organic matter after being produced in the attached organisms[2]。 in addition,when the algae in the periphyton decomposes,the methylmercury in the periphyton can also be released into environmental media such as water or Floc[43]。 In Everglades,Florida,there was a strong correlation between surface water MeHg concentrations and the methylation rate constant of periphyton,（km）,（R2=0.5,P<0.05 )[65]; the fouling organisms in Loxahatchee National Wildlife Refuge(LNWR)and water Conservation Area No.2(WCA2)produce an average of 0.02 and 0.3 kg of methylmercury per day,and these methylmercury account for 10%and 140%of the methylmercury content in the water body,respectively,indicating that the fouling organisms can significantly affect the methylmercury content in the surrounding water body[43,65]。
in general,periphyton is an important primary producer In a variety of aquatic environments and has a strong ability to methylate mercury.the methylmercury produced by periphyton can enter the aquatic food chain or be released into the water body,which has an important impact on the methylmercury levels of aquatic organisms and the water column。

4 Mercury methylation by periphyton

Microbial methylation of inorganic mercury is an intracellular process,so the uptake of inorganic mercury by methylating microorganisms is one of the key processes determining the methylation of bound mercury[9]。 sessile organisms have multi-level microbial structure and functional complexity,and the interaction between different microorganisms blurs the boundaries of metabolites and substrates(such as electron acceptors or electron donors),which is of great significance to the formation and stable development of Sessile organisms[30]。 the periphyton can support the life activities of a variety of mercury methylating bacteria,and the activity and community abundance of mercury methylating bacteria are affected by algae and other bacteria in the periphyton.Therefore,clarifying the bioavailability,microbial activity and related control factors of mercury in periphyton is the key to understanding the methylation of mercury in periphyton and its contribution to methylmercury in the water column and food chain。

4.1 Periphyton can enrich inorganic mercury in aquatic environment and provide substrate for mercury methylation

The production of methylmercury requires inorganic mercury as a reaction substrate.The Bioaccumulation factors(BAFs)of Hg(II)by fouling organisms are as high as 104.5~106.09,suggesting that fouling organisms can provide sufficient substrates for microbial mercury methylation(Fig.1-(1 ))[80,81]。
Attached organisms are rich in EPS secreted by algae and bacteria,which play an important role in the enrichment of mercury[67,82]。 EPS contains a variety of functional groups,such as sulfhydryl(thioglycolic acid,L-cysteine-L-glycine,cysteine,glutathione,etc.),carboxyl,amino,and hydroxyl[49,67][83,84][83,84]。 These functional groups can complex with Hg(II)in water and have a very strong binding capacity with mercury.For example,using three-dimensional fluorescence spectroscopy and Fourier transform infrared spectroscopy,it was found that polysaccharide-like and protein-like substances in EPS had important contributions to mercury binding,and functional groups such as C—N,C—O—C,and P—O played a key role in the binding process[83]。 EPS can be divided into Capsular EPS and colloidal EPS,and there are differences between the two EPS structures.For Colloidal EPS,the ester group is the main functional group binding to mercury;In vesicular EPS,carbon-nitrogen bonds,ether bonds and hydroxyl groups are the main mercury binding sites[83]。 The colloidal EPS located in the outer layer of the attached organism has a stronger adsorption capacity for Hg(II)than the vesicular EPS located in the inner layer,and its binding constant with Hg(II)is 3.47×103and 2.62×103,respectively.In addition,the colloidal EPS is looser,which increases its contact area with the water body.These characteristics make the attached organisms more conducive to the enrichment of Hg(II)in the surrounding water body[83]。 Overall,the strong enrichment ability of EPS for mercury indicates that it can provide sufficient substrate for the methylation of attached biological mercury。
In addition,the enrichment ability of fouling organisms to mercury is also controlled by the type of fouling substrate.For example,in the lake ecosystem,the total mercury concentration in the sediment surface fouling organisms can be as high as 53 980 ng·m-2,which is significantly higher than the fouling organisms（1192 ng·m-2）on the cobblestone surface,and the total mercury in fouling organisms is significantly positively correlated with the total mercury in sediment[85]。 the results suggest that fouling organisms can not only enrich mercury in water,but also adsorb mercury in The fouling matrix。

4.2 Bioavailability of Hg (Ⅱ)

the methylation of mercury by microorganisms does not depend on the total amount of mercury,but on the part that can be absorbed and utilized by microorganisms.The bioavailability of mercury depends on the speciation of mercury.The fouling organisms are rich in EPS secreted by a variety of algae and bacteria,and their functional groups(such as carboxyl,hydroxyl,amino and sulfhydryl)can affect the speciation and bioavailability of mercury through complexation[49,83,84]。 For example,using stannous chloride reduction method,it was found that EPS secreted by attached organisms could significantly reduce the content of active Hg(II)[83]。 Based on the study of Lake Titicaca in South America,it was found that benthic periphyton and periphyton contained a variety of extracellular low-molecular-weight thiols,and there was a significant positive correlation between mercury methylation and total thiol concentration,suggesting that periphyton could promote mercury methylation by secreting low-molecular-weight thiols[67]。 EPS secreted by algae in periphyton is rich in thiol compounds such as cysteine,and the combination of cysteine and mercury can promote the absorption of mercury by thioreductase bacteria,and also enhance the enzymatic synthesis of methylmercury[49][86]。
In addition,the unique redox gradient of periphyton may enhance the bioavailability of mercury.It has been shown that under anoxic conditions,some sulfur-metabolizing microorganisms,such as sulfate-reducing bacteria,can further metabolize thiol compounds in EPS to inorganic sulfur（HS−）,thereby converting Hg(II)to relatively inert mercury sulfide[87,88]。 However,fouling organisms are not completely anoxic,and the interaction between aerobic and anaerobic bacteria may inhibit the formation of mercury sulfide,thereby affecting the bioavailability and methylation of mercury[89]。 For example,purple sulfur bacteria(PSB)and purple non-sulfur bacteria(PNSB)in fouling organisms can convert sulfide to sulfate,thereby converting Hg(II)bound to HS−into more bioavailable forms[47][90]。
the interaction between different microorganisms in the periphyton will affect the spatial structure of the periphyton,thereby affecting the migration rate and bioavailability of mercury[91]。 for example,in the interior of periphyton,there are a large number of polysaccharides,proteins and DNA between cells,and they are distributed in an uneven pattern.These substances usually have a high affinity For mercury,which may affect the migration of mercury in the interior of periphyton[30]。
To sum up,as a multi-species symbiotic environmental medium,the interaction between microorganisms will significantly affect the speciation and bioavailability of mercury。

4.3 Activity of mercury-methylating bacteria

4.3.1 The periphyton can create an anoxic microenvironment for the mercury methylating bacteria to meet their living conditions.

Methylmercury in the environment is mainly produced by anaerobic microorganisms.Therefore,the activity of mercury-methylating microorganisms in fouling organisms is one of the key factors determining their methylation potential.Periphyton can provide survival sites for a variety of mercury-methylating bacteria,such as sulfate-reducing bacteria,iron-reducing geobacteria and methanogens,so that they can be active in the aquatic environment,even in oxygenated surface waters[92][92][93][66]。 the activity of mercury-methylating bacteria varies significantly in different environments,so the types of mercury-methylating bacteria that play a major role in different fouling organisms are also different(Figure 1-(6)).For example,in polluted watersheds,the species with the highest community abundance of mercury methylating bacteria in periphyton are Proteobacteria(25%~55%)and Candidatus Atribacteria(23%~50%)[94]。 There were eight species of bacteria with hgcA gene cluster in the periphyton of hydropower dams and constructed wetlands,among which Geobacillus ferrireducens was the most abundant family[93]。 in lakes near the St.Lawrence River in Canada,methanogens are the main mercury methylating microorganisms in the fouling organisms[66]。
Generally,methylating bacteria are anaerobic bacteria,which are difficult to maintain their life activities and carry out methylation under aerobic conditions.However,there is an obvious redox gradient in the periphyton,from the outer aerobic layer to the inner anoxic layer,including nitrate reduction zone,iron reduction zone,sulfate reduction zone and methanogenic zone[89]。 This unique redox structure within periphyton makes its microbial structure and function very complex[89]。 Therefore,it is speculated that the aerobic bacteria located in the outer layer can form an anoxic microenvironment conducive to the habitat of anaerobic methylating microorganisms by consuming oxygen.For example,in a shallow lake near the St.Lawrence River in Canada,16S rRNA gene sequencing was used to find that aerobic bacteria such as Pseudomonadales and Actinomycetales and anaerobic bacteria such as methanogens were present in the attached organisms on submerged plants[66]。
in addition,fouling organisms are a symbiotic system In which a variety of organisms coexist,and different organisms jointly affect and determine the state of fouling organisms by secreting metabolites or EPS[30]。 As an important component of fouling organisms,EPS is also an important carrier for fouling organisms to express their ecological functions.EPS is rich in a large number of functional groups,which can not only enrich mercury in the water environment,but also provide sufficient nutrients and rich biodiversity for fouling organisms,making various microorganisms in fouling organisms more closely linked and enhancing the interaction between microorganisms[30,82,83,95⇓~97]。 the composition and content of EPS are closely related to the activity of the fouling organism community,and also play an important role in indicating the state of the fouling organism[98]。 in addition,the complex biochemical reactions In fouling organisms can also provide places and conditions conducive to the survival and development of mercury methylating bacteria[99⇓~101]。 It was found that the oxygen and sulfide concentrations in the periphyton had obvious diurnal variation characteristics:no sulfide was found and the oxygen concentration was high in the daytime(up to 1400μmol·L-1）;However,at night,the oxygen concentration can be reduced to 0,while the sulfide concentration can be as high as 50μmol·L-1[100]。 These results suggest that fouling organisms can provide an anoxic microenvironment for methylating bacteria to survive in the aerobic water column through their rich community composition and complex biochemical reactions。

4.3.2 Algae, non-mercury methylating bacteria and particulate matter in periphyton can provide abundant nutrients for methylating bacteria to promote their growth and mercury methylation.

Periphyton has a multi-level microbial community structure,and different microorganisms can share nutrients such as amino acids and bases,so it is speculated that the metabolites secreted by non-methylated microorganisms can provide substrates for methylated microorganisms to stimulate their reproduction and metabolic activity[102,103][104]。
algae in periphyton have an important influence on the activity and abundance of mercury methylating bacteria.Living algae cells can release organic matter(such as DOM,Dissolved organic matter)to the outside world,while dead and lysed algae cells can be directly used as nutrients to promote the growth of bacteria(Figure 1-(4))[105]。 the addition of cyanobacteria to periphyton can significantly increase the yield of methylmercury,suggesting that cyanobacteria can promote the methylation of mercury in periphyton[106][64,106]。 In tropical high-latitude lakes,the concentration of MeHg in fouling organisms was significantly positively correlated with the abundance of Oedogonium cells by（R2=0.783,P=0.0126）[56]。 When algae are destroyed,the mercury methylation of attached organisms will also be inhibited.For example,the methylmercury yield under illumination was reduced by 60%using diuron(DCMU,algae inhibitor)to treat the fouling organisms[53]。 in addition to this,algae can also serve as a secondary habitat for bacteria,protecting bacterial cells In adverse environmental conditions[105]。 Conversely,bacteria can also provide remineralized S,N,and P to promote the growth of algae[105]。 The above studies show that algae in periphyton can significantly affect its methylation。
in addition to the influence of algae,the life activities of mercury-methylating bacteria In periphyton are also controlled by non-mercury-methylating bacteria(Figure 1-(5)).For example,using a variety of specific bacterial inhibitors,it was found that a single inhibition of a certain mercury-methylated bacterial activity did not completely inhibit mercury-methylation;At the same time,mercury methylation can also be reduced by inhibiting some bacteria or algae that are known not to have mercury methylation ability[94]。 the use of fungicides can reduce The mercury methylation ability of fouling organisms by 4%to 72%[45]。 These studies show that various microorganisms in fouling organisms are closely related to each other,and there is frequent material exchange.When the metabolic process of non-mercury methylating bacteria is inhibited,the activity of mercury methylating bacteria will also be reduced.the synergistic effect of different microorganisms in the fouling organism can also promote the production of methylmercury[45,47,90]。 For example,the presence of purple sulfur bacteria and purple non-sulfur bacteria in the fouling organisms can oxidize sulfide to sulfate,thereby promoting the metabolic activity of sulfate-reducing bacteria and mercury methylation;sulfate reducing bacteria reduce sulfate to sulfide,which stimulates the growth of purple sulfur bacteria and purple non-sulfur bacteria[47,90]。
in addition to microorganisms such as algae and non-mercury methylating bacteria,particulate matter is also an important component of periphyton and plays an important role In the formation of periphyton.for example,particulate matter can provide attachment sites For microorganisms such as diatoms,which then gradually develop into attachment communities[28]。 Attached organisms can adsorb or intercept suspended particulate matter in the water environment[107]。 These particles may carry a large amount of nutrients and microorganisms,which will further increase the microbial diversity and community activity of the fouling organisms after entering the fouling organisms.Particulate matter can also affect mercury methylation by affecting the bioavailability of mercury.For example,ferrous sulfide nanoparticles can adsorb Hg(II),resulting in a significant reduction in Hg(II)bioavailability[75]。 Iron oxide particles can effectively concentrate Hg(II)in water environment and improve the bioavailability of Hg(II)[108]。 However,there is still a lack of in-depth research on how particulate matter affects the activity of mercury methylating bacteria and the bioavailability of mercury in periphyton。

5 Conclusion and prospect

Periphyton is an important site of mercury methylation in aquatic environment.its internal spatial structure and rich community composition can enhance the bioavailability of inorganic mercury,improve the activity of mercury methylation bacteria,and then promote the production of methylmercury.Methylmercury produced in fouling organisms is more likely to diffuse to water bodies and enter the food chain,and accumulate in aquatic organisms,which is an important source of methylmercury in the water environment.Therefore,it is of great significance to clarify the mercury methylation of fouling organisms and Its influencing factors for understanding the environmental behavior of mercury.However,at present,most of the studies on mercury enrichment,methylation and bioaccumulation in attached organisms are still phenomena,and the following five aspects need to be strengthened in the future。
(1)the periphyton has a very strong ability to enrich mercury,but there are relatively few studies on the internal mechanism of mercury enrichment by periphyton.Algae and bacteria play an important role in mercury enrichment,but their respective roles in the periphyton system still need to be clarified and distinguished.the unique redox gradient in periphyton is an important reason for the high mercury methylation ability of periphyton,but the reason for the formation and stability of this redox gradient are still unclear。
(2)the mercury methylation rate of fouling organisms is affected by other bacteria inside,but the role of these bacteria in the mercury methylation of fouling organisms is still unclear,and understanding the behavior of these bacteria is of great significance for the analysis of the mercury methylation mechanism of fouling organisms,which needs further exploration in the future。
(3)in addition to lakes,rivers and swamps,periphyton is also widely distributed in paddy fields,which may also play an important role in the enrichment and transformation of mercury in paddy fields.rice is one of the main ways of human exposure to methylmercury,but it is not clear how the fouling organisms affect the methylation and bioaccumulation of mercury in Rice fields[109]。 Therefore,more research is needed to focus on this area in the future。
(4)there are great differences in fouling organisms under different water environments,fouling substrates and nutrient conditions,but There is still a lack of in-depth understanding of the specific roles of different fouling organisms in the environmental transformation of mercury.in order to further understand the behavior of mercury in water environment,future research in this area should be strengthened in order to reduce the harm caused by mercury pollution in water。
(5)periphyton plays an important role in the mercury cycle in the aquatic environment,and is an important place for mercury methylation and an important source of methylmercury for aquatic organisms.Therefore,It is of great significance to control the formation of methylmercury in fouling organisms to reduce the harm of mercury pollution.it is suggested that the demethylation mechanism and key control factors of methylmercury in Periphyton should be further investigated in the future work to reduce mercury pollution in the water environment and effectively prevent the bioaccumulation of methylmercury。

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