%PDF-1.4
%忏嫌
4 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
9 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
19 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
17 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
13 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
12 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
8 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
6 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
20 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
3 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
5 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
22 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
21 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
16 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
7 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
15 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
1 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
18 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
10 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
14 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
11 0 obj
<>>>/BBox[0 0 584.96 782.99]/Length 134>>stream
x0=ю?)-[.T5 /B=屠bKN7(茙aP7{jX枣捑qJ倦;9兼-'羯袿B^:"s)耎荦瞊
徱Yfbs nk诤Q毙%W镪Gk(
endstream
endobj
24 0 obj
<>stream
Metabolic Diversity and Aero-Tolerance in Anammox Bacteria from Geochemically Distinct Aquifers
10.1128/msystems.01255-21
Olivia E. Mosley
Emilie Gios
Louise Weaver
Murray Close
Chris Daughney
Rob van der Raaij
Heather Martindale
Kim M. Handley
Research Article
Research Article
aquifer
groundwater
anammox
鈥淐andidatus Brocadiae鈥
ammonia oxidizers
aero-tolerance
American Society for Microbiology
Mosley et al.
Copyright 漏 2022 Mosley et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.
20220222
2022
ABSTRACT
Anaerobic ammonium oxidation (anammox) is important for converting bioavailable nitrogen into dinitrogen gas, particularly in carbon-poor environments. However, the diversity and prevalence of anammox bacteria in the terrestrial subsurface鈥攁 typically oligotrophic environment鈥攁re little understood. To determine the distribution and activity of anammox bacteria across a range of aquifer lithologies and physicochemistries, we analyzed 16S rRNA genes and quantified hydrazine synthase genes and transcripts sampled from 59 groundwater wells and metagenomes and metatranscriptomes from an oxic-to-dysoxic subset. Data indicate that anammox and anammox-associated bacteria (class 鈥淐andidatus Brocadiae鈥) are prevalent in the aquifers studied, and that anammox community composition is strongly differentiated by dissolved oxygen (DO), but not ammonia/nitrite. While 鈥淐andidatus Brocadiae鈥 diversity decreased with increasing DO, 鈥淐andidatus Brocadiae鈥 16S rRNA genes and hydrazine synthase (hzsB) genes and transcripts were detected across a wide range of bulk groundwater DO concentrations (0 to 10鈥塵g/L). Anammox genes and transcripts correlated significantly with those involved in aerobic ammonia oxidation (amoA), potentially representing a major source of nitrite for anammox. Eight 鈥淐andidatus Brocadiae鈥 genomes (63 to 95% complete), representing 2 uncharacterized families and 6 novel species, were reconstructed. Six genomes have genes characteristic of anammox, all for chemolithoautotrophy. Anammox and aerotolerance genes of up to four 鈥淐andidatus Brocadiae鈥 genomes were transcriptionally active under oxic and dysoxic conditions, although activity was highest in dysoxic groundwater. The coexpression of nrfAH nitrite reductase genes by 鈥淐andidatus Brocadiae鈥 suggests active regeneration of ammonia for anammox. Our findings indicate that anammox bacteria contribute to loss of fixed N across diverse anoxic-to-oxic aquifer conditions, which is likely supported by nitrite from aerobic ammonia oxidation.
IMPORTANCE Anammox is increasingly shown to play a major role in the aquatic nitrogen cycle and can outcompete heterotrophic denitrification in environments low in organic carbon. Given that aquifers are characteristically oligotrophic, anammox may represent a major route for the removal of fixed nitrogen in these environments, including agricultural nitrogen, a common groundwater contaminant. Our research confirms that anammox bacteria and the anammox process are prevalent in aquifers and occur across diverse lithologies (e.g., sandy gravel, sand-silt, and volcanic) and groundwater physicochemistries (e.g., various oxygen, carbon, nitrate, and ammonium concentrations). Results reveal niche differentiation among anammox bacteria largely driven by groundwater oxygen contents and provide evidence that anammox is supported by proximity to oxic niches and handoffs from aerobic ammonia oxidizers. We further show that this process, while anaerobic, is active in groundwater characterized as oxic, likely due to the availability of anoxic niches.
20211015
20220118
2379-5077
Adobe LiveCycle PDF Generator; modified using iText庐 5.5.13.2 漏2000-2020 iText Group NV (AGPL-version)2023-05-02T16:18:58-07:00
endstream
endobj
25 0 obj
<>stream
x+ |
endstream
endobj
26 0 obj
<>stream
x淪**T0T0 B櫆珷慽d犩挴 vU
endstream
endobj
27 0 obj
<>stream
x+ |
endstream
endobj
28 0 obj
<>stream
x淪**T0T0 B櫆珷慽∴挴 y+
endstream
endobj
29 0 obj
<>stream
x+ |
endstream
endobj
30 0 obj
<>stream
x淪**T0T0 B櫆珷慽⑧挴 y\'
endstream
endobj
31 0 obj
<>stream
x+ |
endstream
endobj
32 0 obj
<>stream
x淪**T0T0 B櫆珷慽h挴 W
endstream
endobj
33 0 obj
<>stream
x+ |
endstream
endobj
34 0 obj
<>stream
x淪**T0T0 B櫆珷慽h⑧挴 X
endstream
endobj
35 0 obj
<>stream
x+ |
endstream
endobj
36 0 obj
<>stream
x淪**T0T0 B櫆珷慽h∴挴 \
endstream
endobj
37 0 obj
<>stream
x+ |
endstream
endobj
38 0 obj
<>stream
x淪**T0T0 B櫆珷慽挴 ye(
endstream
endobj
39 0 obj
<>stream
x+ |
endstream
endobj
40 0 obj
<>stream
x淪**T0T0 B櫆珷慽む挴 yJ%
endstream
endobj
41 0 obj
<>stream
x+ |
endstream
endobj
42 0 obj
<>stream
x淪**T0T0 B櫆珷慽ㄠ挴 yA$
endstream
endobj
43 0 obj
<>stream
x+ |
endstream
endobj
44 0 obj
<>stream
x淪**T0T0 B櫆珷慽┼挴 y,
endstream
endobj
45 0 obj
<>stream
x+ |
endstream
endobj
46 0 obj
<>stream
x淪**T0T0 B櫆珷慽h犩挴 lT
endstream
endobj
47 0 obj
<>stream
x+ |
endstream
endobj
48 0 obj
<>stream
x淪**T0T0 B櫆珷慽挴 yw*
endstream
endobj
49 0 obj
<>stream
x+ |
endstream
endobj
50 0 obj
<>stream
x淪**T0T0 B櫆珷慽hむ挴 ~V
endstream
endobj
51 0 obj
<>stream
x+ |
endstream
endobj
52 0 obj
<>stream
x淪**T0T0 B櫆珷慽h挴 [
endstream
endobj
53 0 obj
<>stream
x+ |
endstream
endobj
54 0 obj
<>stream
x淪**T0T0 B櫆珷慽dㄠ挴 V
endstream
endobj
55 0 obj
<>stream
x+ |
endstream
endobj
56 0 obj
<>stream
x淪**T0T0 B櫆珷慽挴 yS&
endstream
endobj
57 0 obj
<>stream
x+ |
endstream
endobj
58 0 obj
<>stream
x淪**T0T0 B櫆珷慽h┼挴 ]
endstream
endobj
59 0 obj
<>stream
x+ |
endstream
endobj
60 0 obj
<>stream
x淪**T0T0 B櫆珷慽hㄠ挴 uU
endstream
endobj
61 0 obj
<>stream
x+ |
endstream
endobj
62 0 obj
<>stream
x淪**T0T0 B櫆珷慽︵挴 yn)
endstream
endobj
63 0 obj
<>stream
x+ |
endstream
endobj
64 0 obj
<>stream
x淪**T0T0 B櫆珷慽h挴 Y
endstream
endobj
65 0 obj
<>stream
x+ |
endstream
endobj
66 0 obj
<>stream
x淪**T0T0 B櫆珷慽h︵挴 Z
endstream
endobj
69 0 obj
<>stream
x湆\S勺陆択\L 鰡4+牏倛綏袐Q傯"*HM盎脍Ww]水浑篹nv鸱镘抹跨y鼾爓鏋欩3g9g顒牤莃眴害茋I僔徘Lu MdhSi=桗nw峪t鬦n9瞀扇q>G馳
G蟈彲7B蟎o傓T=k靳z蝯+踔鑩轾雲肱%辚雖宜+勋;⒆プZ铫辵禁z/魚襸7纫c,cK虤虏b蚦9矕諽謚=謈+/?X9鶦魢閶鬐隣苑詿ワǹL進逽遊_/紫邢者痏_く酗蠾闊湛[;鷲蚥s${{<{*蹫=燀腲臹琐e嚤撠╈l.鯺v%粸菽ngw丙贄7龠部g縡师
L2o0賎殎嵙K
V2Xk稗浪`爜 莁汚橝滱揂妨y冿黬疝 bl寖 Fbf嘙&a1+泹兔湴ヘr[峬腂盭,蹎砼*&粓=戮寝`1郈疳焾侠g銕顗!x,瀶o苭
迠w鉭+鴐1#+8z##鈱錖遑qp9/N '挀纳怃r鰌qj99渵巫滬滅湡8p
1C炨W嗘啌:53L3躡榦XdXix园桶丘U;哋_H睂#襤ぱ8#KF崠
5J0J3赿从h!&KFF=5璀F,'IS +b>酓7H馜6慜'J袹ty*q媥@<#^僜6椸歳透顇頣
w讈粚粖粠胨晀# 4&n! 穫{榹湯圉pOs/r酷掊>纩例夳;楁⺧1f,2m<蓌厚L泫茓峕=尳尌啤1苧鉒悱苹岟26>j躡|赂哮滖灼W噭I)0&*J*
擡'.
垪蒭嫝1褘bBbKe広g8喤&EG蔙僢祄4ENē4qg眴缠S嵟Z芘!嫷蠯5諙~F[鷧,K?祍惼;L觠衮eZ竐Z琫塧慉插煫薊#紜F/閳荍M貸M偈/受4l蹷摙CゑIQ懸7-G穭HiBé賘鞸觴=4t廆YPXdぴ愠T_TZ凓礔觮TO
_/鵽j鵽j{猢轭:
泆熱吷鈋 a 隑猊r賳%4/M疧猐)'瞻昷9I禍2M魼鞸#i鄃睦Om4EA殹梚pd婌S
W"覤噃獏|F鵅!熩"厏觔卛tZX#5駾~IG<5e褮茶/蔮4lb-菢螩瘆j8ACO8 煡JR"闣ⅵi$
撙/&i&i{毮}挦簧6蔁釗uC煬樵%B殾A'誇勀薲褢诣牥纇ilLBb|Ll,戦J蟛(26T K."I漝憠遗 a1裗埜8Q祾.C+け盧iT@愒5ie寅0法0F鶸a獵c<翨ⅳk炡东BC肰%:﹩噯跥hm>QKc?et瞹闹=縣1傋HHAL?d诤i垐%2C,"榽Dj鷳6葳1:)%,F06,>4&侀L4)I嗱17椐稳緪K霰a1_dtR苵褭/%齱gb>u嫠WM-扪J撎\,崕AA&噮蜆>}芁]芧棛1c5齝芕棻殹薠26簩.c钀璽萔:dk牭衂hm钀璾戎:dk驳賈噇堆!坭恗t6:d矋貴噇儿
]s[箔裒S賄噇獵墩!坳恗u葀:欗t葀慻|捫頢Fh从我e靦3u3u⑽詨:S'闘騆騆騆郘牻衈'賌噇疌蹲!垭愴u撒:d{,,,,,,,颥O2jeu簩N接璾]芕棻觘f2龊yY'〗嵼$d袐+m哽fX踆懙J泞?L誸回鴺牑滥$%!+俈t42,:8,:,15橫磗G⑼(>&E$峝V0揊4磭#靫-1&嵄|駫臢赿&Y2C沊ikmb玀f.液w岓鰍笮菟R茍h蝊'W峺
L峸`LJ ┅坁>拑礵%翼Q儰{褦 墫豗踙{m2K89jim驊瑜Mk%毮f6櫋M壍6裷氨&v赿6巡笛驳羊逞虺羊逞2惭2舱2舱2舱2舱2舱2舱2舱2舱2舱2舱2舱2舱2舱2舱v蘓讼V讼N讼J畚J畚J畚J畚J畚N+挐V$;璈vZ戩"賗E灿奷蒒m队B踼勚蔮臵+嫷枒禆"m旹****ZY床8heq惺鉅暸A+媰V,ZY床8|w隸筐`?魀寜M峠'N2窔>}葫 櫣GjrA虠!//>6&瀁彇鎷"#蚖3蘔d駌嗚i閍i
U圢4w%X毲蕫Q痹瀆槆%楰豌e!饶d瀳V-騨#蘡q|U|尮骠泱粸9諼瑮畐U廸峛叢n?搈螢蔨eAa齠僙K荍癑2n剰歧>
殐97
0紀dk辞ㄎ,aFX+圠"忚@!鏟異k溯容梯私媒淆秦葂8c?鉘1~c!鍯靽D2缺!MC
鵨萠CM鋣瘘y踶M<,%颳#3摴&M\M謿l47 71)09dRor啼偵5撟C鯂RC韲.簗ㄧ
C}嚘;磓╮枵嚲T逿`:賢鹃jS/ $L汳跰鸏瘺>5熋7艞鹎'螫|?~_蜗鄌餕鵊黱~#噽$9KN#g搵蒭90
F`3侰8蝺B儊 ~fK
hm
0!y
鏧羜蠪L顑%`聦哙葏z印=滭骴0攊;i翉励齓&靸C绍$軆X2鑾n*貧+転-w8auD`BBtldZ骆褸硟-囑廮9垴苽讨阈^蕱m憞on萊d5C>孠%坚)<%7e{嗀[巨k比"廪P
弒嗖鲬棡=誡'.拦澰%鰼牁炧=8g蟱鏫鹏帆V恷+獹羲粘O铠(5J vW\R5棆+Xy偓腛d蛊m眥(葽恬樀
!鼉仕饽潮<\櫦駭卙苑唖郬螰!舷u,裴h噓鉣7V詣売dXL邾坛3譐OtI旐鯒壭i;R阀嫍苹Al鮧葲O乜nu昫Of~F獝K忶Z溇Z賡 >喇й23k%
$斋|3N卌_鉀E説KvVT韓郏8v陌疋s/.溄n欍奛;Me
礖s[糝C3胹S2v驿O棊x:m俟mG$.=2%H挹」玂聥蕻虜僕
pHG⒕膥矖L{<滌輞D憑R趔澥頽I民g匑叨ou墄7囲讹聙鎴=xM臠飉沞U劆按~w楄粉a媀篛扡聝炨d镞/}FA武啾!冰吷迻9hFmL黢#卩8 8@\鲧 黢p8墬.踼P|ヲ傟询蛃%癕:8騤}姝赭玑\$坅J|0寃`K懧 /+埒&檘O鈀n伇7宸U'!籟2馆魁t跰篮袡扷!
t*.@ <