Microbial communities in sediment from Zostera marina patches, but not the Z. marina leaf or root microbiomes, vary in relation to distance from patch edge

PeerJ

Volumn 2017, Issue 4, 2017, Pages

  Ettinger, Cassandra L ^a   Voerman, Sofie E ^b   Lang, Jenna M ^a,c   Stachowicz, John J ^a   Eisen, Jonathan A ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c Trace Genomics   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Edge effect; Eelgrass; Fragmentation; Microbiome; Rhizosphere; Seagrass; Sulfur metabolism

Indexed keywords

ALISMATALES; ALTEROMONADALES; ARTICLE; BACTEROIDALES; CHROMATIALES; CLOSTRIDIALES; DESULFOBACTERALES; DESULFUROMONADALES; FLAVOBACTERALES; FLAVOBACTERIALES; GENE SEQUENCE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; POLYMERASE CHAIN REACTION; RHIZOSPHERE; RHODOBACTERALES; SAPROSPIRALES; TAXONOMY; THIOTRICHALES; ZOSTERA MARINA;

EID: 85018181732     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.3246     Document Type: Article

References (98)

1. Adhitya A, Thomas FIM, Ward BB. 2007. Diversity of assimilatory nitrate reductase genes from plankton and epiphytes associated with a seagrass bed. Microbial Ecology 54:587-597 DOI 10.1007/s00248-006-9175-0.
2. Aleklett K, Leff JW, Fierer N, Hart M. 2015. Wild plant species growing closely connected in a subalpine meadow host distinct root-associated bacterial communities. PeerJ 3:e804 DOI 10.7717/peerj.804.
3. Alexiev A, Krusor ML, Jospin G, Lang JM, Eisen JA, Coil DA. 2016a. Draft genome sequences of two Pseudoalteromonas strains isolated from roots and leaf blades of the seagrass Zostera marina. Genome Announcements 4(1):e00010-16 DOI 10.1128/genomeA.00010-16.
4. Alexiev A, Krusor ML, Jospin G, Lang JM, Eisen JA, Coil DA. 2016b. Draft genome sequence of Cobetia sp. UCD-24C, isolated from roots and leaves of the seagrass Zostera marina. Genome Announcements 4(2):e00116-16 DOI 10.1128/genomeA.00116-16.
5. Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32-46.
6. Anderson MJ, Walsh DC. 2013. PERMANOVA, ANOSIM, and the mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecological Monographs 83:557-574 DOI 10.1890/12-2010.1.
7. Bagwell CE, Rocque JR, Smith GW, Polson SW, Friez MJ, Longshore JW, Lovell CR. 2002. Molecular diversity of diazotrophs in oligotrophic tropical seagrass bed communities. FEMS Microbiology Ecology 39:113-119 DOI 10.1111/j.1574-6941.2002.tb00912.x.
8. Barber TR, Carlson PR. 1993. Effects of seagrass die-off on benthic fluxes and porewater concentrations of Σ CO2, Σ H2S, and CH4 in Florida Bay Sediments. In: Oremland RS, ed. Biogeochemistry of global change: radiatively active trace gases. New York: Chapman and Hall, 530-550.
9. Beckers B, OP De Beeck M, Weyens N, Van Acker R, Van Montagu M, Boerjan W, Vangronsveld J. 2016. Lignin engineering in field-grown poplar trees affects the endosphere bacterial microbiome. Proceedings of the National Academy of Sciences of the United States of America 113:2312-2317 DOI 10.1073/pnas.1523264113.
10. Bent SJ, Forney LJ. 2008. The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. The ISME Journal 2:689-695 DOI 10.1038/ismej.2008.44.
11. Bos AR, Bouma TJ, De Kort GLJ, Van Katwijk MM. 2007. Ecosystem engineering by annual intertidal seagrass beds: sediment accretion and modification. Estuarine, Coastal and Shelf Science 74:344-348 DOI 10.1016/j.ecss.2007.04.006.
12. Bouffaud ML, Poirier MA, Muller D, Moënne-Loccoz Y. 2014. Root microbiome relates to plant host evolution in maize and other Poaceae. Environmental Microbiology 16:2804-2814 DOI 10.1111/1462-2920.12442.
13. Bowen JL, Morrison HG, Hobbie JE, Sogin ML. 2012. Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates. The ISME Journal 6:2014-2023 DOI 10.1038/ismej.2012.47.
14. Bray JR, Curtis JT. 1957. An ordination of the upland forest communities of Southern Wisconsin. Ecological Monographs 27:325-349 DOI 10.2307/1942268.
15. Caffrey JM, Kemp WM. 1991. Seasonal and spatial patterns of oxygen production, respiration and root-rhizome release in Potamogeton perfoliatus L. and Zostera marina L. Aquatic Botany 40:109-128 DOI 10.1016/0304-3770(91)90090-R.
16. Campbell BJ, Engel AS, Porter ML, Takai K. 2006. The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nature Reviews. Microbiology 4:458-468 DOI 10.1038/nrmicro1414.
17. Capone DG. 1982. Nitrogen fixation (Acetylene Reduction) by rhizosphere sediments of the eelgrass Zostera marina. Marine Ecology Progress Series 10:67-75 DOI 10.3354/meps010067.
18. Capone DG, Budin JM. 1982. Nitrogen fixation associated with rinsed roots and rhizomes of the eelgrass Zostera marina. Plant Physiology 70:1601-1604 DOI 10.1104/pp.70.6.1601.
19. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7:335-336 DOI 10.1038/nmeth.f.303.
20. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. 2012. Ultrahigh-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6:1621-1624.
21. Cebrián J, Pedersen MF, Kroeger KD, Valiela I. 2000. Fate of production of the seagrass Cymodocea nodosa in different stages of meadow formation. Marine Ecology Progress Series 204:119-130 DOI 10.3354/meps204119.
22. Chao A. 1984. Non-parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, Theory and Applications 11:265-270.
23. Chaparro JM, Badri DV, Vivanco JM. 2014. Rhizosphere microbiome assemblage is affected by plant development. The ISME Journal 8:790-803 DOI 10.1038/ismej.2013.196.
24. Cleary DFR, Polónia ARM, Sousa AI, Lillebø AI, Queiroga H, Gomes NCM. 2016. Temporal dynamics of sediment bacterial communities in monospecific stands of Juncus maritimus and Spartina maritima. Plant Biology 18:824-834 DOI 10.1111/plb.12459.
25. Connell EL, Colmer TD, Walker DI. 1999. Radial oxygen loss from intact roots ofHalophila ovalisas a function of distance behind the root tip and shoot illumination. Aquatic Botany 63:219-228 DOI 10.1016/S0304-3770(98)00126-0.
26. Cúcio C, Engelen AH, Costa R, Muyzer G. 2016. Rhizosphere microbiomes of European seagrasses are selected by the plant, but are not species specific. Frontiers in Microbi-ology 7:440 DOI 10.3389/fmicb.2016.00440.
27. Dang H, Li T, Chen M, Huang G. 2008. Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Applied and Environmental Microbiology 74:52-60 DOI 10.1128/AEM.01400-07.
28. Dauby P, Bale AJ, Bloomer N, Canon C, Ling RD, Norro A, Robertson JE, Simon A, Théate JM, Watson AJ, Frankignoulle M. 1995. Particle fluxes over a Mediterranean seagrass bed: a one year case study. Marine Ecology Progress Series 126:233-246 DOI 10.3354/meps126233.
29. Davies-Colley RJ, Payne GW, Van Elswijk M. 2000. Microclimate gradients across a forest edge. New Zealand Journal of Ecology 11:1-121.
30. De Boer WF. 2007. Seagrass-sediment interactions, positive feedbacks and critical thresholds for occurrence: a review. Hydrobiologia 591:5-24 DOI 10.1007/s10750-007-0780-9.
31. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Micro-biology 72:5069-5072 DOI 10.1128/AEM.03006-05.
32. Dixon P. 2003. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science: Official Organ of the International Association for Vegetation Science 14:927-930 DOI 10.1111/j.1654-1103.2003.tb02228.x.
33. Duarte CM, Borum K, Short FT, Walker DI. 2005. Seagrass ecosystems: their global status and prospects. In: Polunin NVC, ed. Aquatic ecosystems: trends and global prospects. Cambridge Univ., 281-294.
34. Duarte CM, Cebrián J. 1996. The fate of marine autotrophic production. Limnology and Oceanography 41:1758-1766 DOI 10.4319/lo.1996.41.8.1758.
35. Duarte CM, Holmer M, Marbà N. 2005. Plant-microbe interactions in seagrass meadows. Coastal and Estuarine Studies Epub ahead of print Mar 23 2013 DOI 10.1029/CE060p0031.
36. Duarte CM, Sand-Jensen K. 1990. Seagrass colonization: patch formation and patch growth in Cymodocea nodosa. Marine Ecology Progress Series 65:193-200 DOI 10.3354/meps065193.
37. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinfor-matics 26:2460-2461 DOI 10.1093/bioinformatics/btq461.
38. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proceedings of the National Academy of Sciences of the United States of America 112:E911-E920 DOI 10.1073/pnas.1414592112.
39. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T. 2013. The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiology Reviews 37:462-476 DOI 10.1111/1574-6976.12011.
40. Elser JJ, Bracken MES, Clel EE, Gruner DS, Harpole WS, Hillebr H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10:1135-1142 DOI 10.1111/j.1461-0248.2007.01113.x.
41. Erskine JM, Koch MS. 2000. Sulfide effects on Thalassia testudinum carbon balance and adenylate energy charge. Aquatic Botany 67:275-285 DOI 10.1016/S0304-3770(00)00099-1.
42. Flaspohler DJ, Temple SA, Rosenfield RN. 2001. Species-specific edge effects on nest success and breeding bird density in a forested landscape. Ecological Applications 11:32-46 DOI 10.2307/3061053.
43. Folkard AM. 2005. Hydrodynamics of modelPosidonia oceanicapatches in shallow water. Limnology and Oceanography 50:1592-1600 DOI 10.4319/lo.2005.50.5.1592.
44. Fonseca MS, Fisher JS, Zieman JC, Thayer GW. 1982. Influence of the seagrass, Zostera marina L. on current flow. Estuarine, Coastal and Shelf Science 15:351-364 DOI 10.1016/0272-7714(82)90046-4.
45. Fox BJ, Taylor JE, Fox MD, Williams C. 1997. Vegetation changes across edges of rainforest remnants. Biological Conservation 82:1-13 DOI 10.1016/S0006-3207(97)00011-6.
46. Gacia E, Esperança G, Duarte CM, Middelburg JJ. 2002. Carbon and nutrient deposition in a Mediterranean seagrass (Posidonia oceanica) meadow. Limnology and Oceanog-raphy 47:23-32 DOI 10.4319/lo.2002.47.1.0023.
47. Garrity GM, Bell JA, Lilburn T. 2005. Order V. Thiotrichales ord nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM, eds. Bergey's manual of systematic bacteriology (The Proteobacteria), Part B (The Gammaproteobacteria). Vol. 2. New York: Springer, 131.
48. Gomes NCM, Cleary DFR, Pinto FN, Egas C, Almeida A, Cunha A, Mendonça-Hagler LCS, Smalla K. 2010. Taking root: enduring effect of rhizosphere bacterial colonization in mangroves. PLOS ONE 5(11):e14065 DOI 10.1371/journal.pone.0014065.
49. Granata TC, Serra T, Colomer J, Casamitjana X, Duarte CM, Gacia E. 2001. Flow and particle distributions in a nearshore seagrass meadow before and after a storm. Marine Ecology Progress Series 218:95-106 DOI 10.3354/meps218095.
50. Hamady M, Lozupone C, Knight R. 2010. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. The ISME Journal 4:17-27 DOI 10.1038/ismej.2009.97.
51. Harrison S, Bruna E. 1999. Habitat fragmentation and large-scale conservation: what do we know for sure? Ecography 22:225-232 DOI 10.1111/j.1600-0587.1999.tb00496.x
52. Hollants J, Leliaert F, De Clerck O, Willems A. 2013. What we can learn from sushi: a review on seaweed-bacterial associations. FEMS Microbiology Ecology 83:1-16 DOI 10.1111/j.1574-6941.2012.01446.x
53. Jensen SI, Kühl M, Priemé A. 2007. Different bacterial communities associated with the roots and bulk sediment of the seagrass Zostera marina. FEMS Microbiology Ecology 6:108-117.
54. Jiang YF, Ling J, Dong JD, Chen B, Zhang YY, Zhang YZ, Wang YS. 2015. Illuminabased analysis the microbial diversity associated with Thalassia hemprichii in Xincun Bay, South China Sea. Ecotoxicology 24:1548-1556 DOI 10.1007/s10646-015-1511-z.
55. Koch EW. 2001. Beyond light: physical, geological, and geochemical parameters as possible submersed aquatic vegetation habitat requirements. Estuaries 24:1-17 DOI 10.2307/1352808.
56. Kou W, Zhang J, Lu X, Ma Y, Mou X, Wu L. 2016. Identification of bacterial communities in sediments of Poyang Lake, the largest freshwater lake in China. SpringerPlus 5:401 DOI 10.1186/s40064-016-2026-7.
57. Kramer CY. 1956. Extension of multiple range tests to group means with unequal numbers of replications. Biometrics 12:307-310 DOI 10.2307/3001469.
58. Kramer CY. 1957. Extension of multiple range tests to group correlated adjusted means. Biometrics 13:13-18 DOI 10.2307/3001898.
59. Lakshmanan V. 2015. Root microbiome assemblage is modulated by plant host factors. In: Bais H, Sherrier J, eds. Plant microbe interactions. Advances in botanical research. Vol. 75, 57-79.
60. Lamers LPM, Govers LL, Janssen ICJM, Geurts JJM, Van der Welle MRW, Van Katwijk MM, Van der Heide T, Roelofs JGM, Smolders AJP. 2013. Sulfide as a soil phytotoxin-a review. Frontiers in Plant Science 4:Article 268 DOI 10.3389/fpls.2013.00268.
61. Lang JM, Eisen JA, Zivkovic AM. 2014. The microbes we eat: abundance and taxonomy of microbes consumed in a day's worth of meals for three diet types. PeerJ 2:e659 DOI 10.7717/peerj.659.
62. Lee RD, Jospin G, Lang JM, Eisen JA, Coil DA. 2015a. Draft genome sequence of Pseudoalteromonas tetraodonis Strain UCD-SED8 (Phylum Gammaproteobacteria). Genome Announcements 3(6):e01276-15 DOI 10.1128/genomeA.01276-15.
63. Lee RD, Jospin G, Lang JM, Eisen JA, Coil DA. 2015b. Draft genome sequence of Bacillus vietnamensis Strain UCD-SED5 (Phylum Firmicutes). Genome Announcements 3(6):e01376-15 DOI 10.1128/genomeA.01376-15.
64. Lee RD, Jospin G, Lang JM, Eisen JA, Coil DA. 2016a. Draft genome sequences of two Vibrio splendidus strains, isolated from seagrass sediment. Genome Announcements 4(1):e01769-15 DOI 10.1128/genomeA.01769-15.
65. Lee RD, Jospin G, Lang JM, Eisen JA, Coil DA. 2016b. Draft genome sequences of two Pseudoalteromonas porphyrae strains isolated from seagrass sediment. Genome Announcements 4(2):e00092-16 DOI 10.1128/genomeA.00092-16.
66. Les DH, Cleland MA, Waycott M. 1997. Phylogenetic studies in alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Systematic Botany 22:443-463 DOI 10.2307/2419820.
67. Lovell CR. 2002. Plant-microbe interactions in the marine environment. In: Bitton G, ed. Encyclopedia of environmental microbiology. Vol. 5. Hoboken: Wiley, 2539-2554.
68. Lozupone CA, Hamady M, Kelley ST, Knight R. 2007. Quantitative and qualitative diversity measures lead to different insights into factors that structure microbial communities. Applied and Environmental Microbiology 73:1576-1585 DOI 10.1128/AEM.01996-06.
69. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-90 DOI 10.1038/nature11237.
70. Malmivaara-Lämsä M, Hamberg L, Haapamäki E, Liski J, Kotze DJ, Lehvävirta S, Fritze H. 2008. Edge effects and trampling in boreal urban forest fragments-impacts on the soil microbial community. Soil Biology & Biochemistry 40:1612-1621 DOI 10.1016/j.soilbio.2008.01.013.
71. McClung CR, Patriquin DG. 1980. Isolation of a nitrogen-fixing Campylobacter species from the roots of Spartina alterniflora Loisel. Canadian Journal of Microbiology 26:881-886 DOI 10.1139/m80-153.
72. McMurdie PJ, Holmes S. 2013. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLOS ONE 8(4):e61217 DOI 10.1371/journal.pone.0061217.
73. Mejia AY, Rotini A, Lacasella F, Bookman R, Thaller MC, Shem-Tov R, Winters G, Migliore L. 2016. Assessing the ecological status of seagrasses using morphology, biochemical descriptors and microbial community analyses. A study in Halophila Stipulacea (Forsk.) Aschers meadows in the northern Red Sea. Ecological Indicators 60:1150-1163.
74. Nielsen LB, Finster K, Welsh DT, Donelly A, Herbert RA, De Wit R, Lomstein BA. 2001. Sulphate reduction and nitrogen fixation rates associated with roots, rhizomes and sediments from Zostera noltii and Spartina maritima meadows. Environmental Microbiology 3:63-71 DOI 10.1046/j.1462-2920.2001.00160.x.
75. Olsen JL, Rouzé P, Verhelst B, Lin Y-C, Bayer T, Collen J, Dattolo E, De Paoli E, Dittami S, Maumus F, Michel G, Kersting A, Lauritano C, Lohaus R, Töpel M, Tonon T, Vanneste K, Amirebrahimi M, Brakel J, Boström C, Chovatia M, Grimwood J, Jenkins JW, Jueterbock A, Mraz A, Stam WT, Tice H, Bornberg-Bauer E, Green PJ, Pearson GA, Procaccini G, Duarte CM, Schmutz J, Reusch TBH, Van de Peer Y. 2016. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530:331-335 DOI 10.1038/nature16548.
76. Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes RA, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL. 2006. A global crisis for seagrass ecosystems. Bioscience 56:987-996 DOI 10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2.
77. Palacios R, Newton WE. 2005. Genomes and genomics of nitrogen-fixing organisms. Dordrecht: Springer.
78. Paton PWC. 1994. The effect of edge on avian nest success: how strong is the evidence? Conservation Biology: the Journal of the Society for Conservation Biology 8:17-26 DOI 10.1046/j.1523-1739.1994.08010017.x.
79. Pedersen O, Borum J, Duarte CM, Fortes MD. 1998. Oxygen dynamics in the rhizosphere of Cymodocea rotundata. Marine Ecology Progress Series 169:283-288 DOI 10.3354/meps169283.
80. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the United States of America 110:6548-6553 DOI 10.1073/pnas.1302837110.
81. R Core Team. 2016. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at https://www.r-project.org. Ricart AM, York PH, Rasheed MA, Pérez M, Romero J, Bryant CV, Macreadie PI. 2015.
82. Ricart AM, York PH, Rasheed MA, Pérez M, Romero J, Bryant CV, Macreadie PI. 2015. Variability of sedimentary organic carbon in patchy seagrass landscapes. Marine Pollution Bulletin 100:476-482 DOI 10.1016/j.marpolbul.2015.09.032.
83. Roth-Schulze AJ, Zozaya-Valdés E, Steinberg PD, Thomas T. 2016. Partitioning of functional and taxonomic diversity in surfaceêassociated microbial communities. Environmental Microbiology 18:4391-4402 DOI 10.1111/1462-2920.13325.
84. Shannon CE, Weaver W. 1949. The mathematical theory of communication. Urbana: University of Illinois Press, 29.
85. Short FT. 1987. Effects of sediment nutrients on seagrasses: literature review and mesocosm experiment. Aquatic Botany 27:41-57 DOI 10.1016/0304-3770(87)90085-4.
86. Short FT, Short CA. 1984. The seagrass filter: purification of estuarine and coastal waters. In: Kennedy VS, ed. The estuary as a filter. Orlando: Acadamic Press, 395-413.
87. Simpson EH. 1949. Measurement of diversity. Nature 163:688-688 DOI 10.1038/163688a0.
88. Smith TM, Hindell JS, Jenkins GP, Connolly RM. 2008. Edge effects on fish associated with seagrass and sand patches. Marine Ecology Progress Series 359:203-213 DOI 10.3354/meps07348.
89. Smith TM, Hindell JS, Jenkins GP, Connolly RM, Keough MJ. 2011. Edge effects in patchy seagrass landscapes: the role of predation in determining fish distribution. Journal of Experimental Marine Biology and Ecology 399:8-16 DOI 10.1016/j.jembe.2011.01.010.
90. Sun F, Zhang X, Zhang Q, Liu F, Zhang J, Gong J. 2015. Seagrass (Zostera marina) colonization promotes the accumulation of diazotrophic bacteria and alters the relative abundances of specific bacterial lineages involved in benthic carbon and sulfur cycling. Applied and Environmental Microbiology 81:6901-6914 DOI 10.1128/AEM.01382-15.
91. Tanner JE. 2005. Edge effects on fauna in fragmented seagrass meadows. Austral Ecology 30:210-218 DOI 10.1111/j.1442-9993.2005.01438.x.
92. Terrados J, Duarte CM, Kamp-Nielsen L, Agawin NSR, Gacia E, Lacap D, Fortes MD, Borum J, Lubanski M, Greve T. 1999. Are seagrass growth and survival constrained by the reducing conditions of the sediment? Aquatic Botany 65:175-197 DOI 10.1016/S0304-3770(99)00039-X.
93. Thomas F, Giblin AE, Cardon ZG, Sievert SM. 2014. Rhizosphere heterogeneity shapes abundance and activity of sulfur-oxidizing bacteria in vegetated salt marsh sediments. Frontiers in Microbiology 5:Article 309.
94. Tukey JW. 1953. The problem of multiple comparisons. The collected works of John W. Tukey, vol. 8. New York: Chapman & Hall.
95. Van der Heide T, Govers LL, De Fouw J, Olff H, Van Der Geest M, Van Katwijk MM, Piersma T, Van de Koppel J, Silliman BR, Smolders AJP, Van Gils JA. 2012. A three-stage symbiosis forms the foundation of seagrass ecosystems. Science 336:1432-1434 DOI 10.1126/science.1219973.
96. Warton DI, Wright ST, Wang Y. 2012. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution 3:89-101 DOI 10.1111/j.2041-210X.2011.00127.x.
97. Welsh DT. 2000. Nitrogen fixation in seagrass meadows: regulation, plant-bacteria interactions and significance to primary productivity. Ecology Letters 3:58-71 DOI 10.1046/j.1461-0248.2000.00111.x.
98. Wickham H. 2009. ggplot2: elegant graphics for data analysis. New York: Springer-Verlag. Williams SL, Heck Jr KL. 2001. Seagrass communities ecology. In: Bertness MD, Gaines SD, Hay ME, eds. Marine community ecology. Sunderland: Sinauer Associates, 317-337.