Differences in structure of northern Australian hypolithic communities according to location, rock type, and gross morphology

Susannah P. Guenther; Karen S. Gibb; Alea M. Rose; Mirjam Kaestli; Keith A. Christian; Susannah P. Guenther; Karen S. Gibb; Alea M. Rose; Mirjam Kaestli; Keith A. Christian

doi:10.3934/microbiol.2018.3.469

AIMS Microbiology

2018, Volume 4, Issue 3: 469-481. doi: 10.3934/microbiol.2018.3.469

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Differences in structure of northern Australian hypolithic communities according to location, rock type, and gross morphology

Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia

Received: 20 April 2018 Accepted: 19 June 2018 Published: 25 June 2018

Hypolithic communities (under translucent rocks) were compared between a semi-arid site (Wave Hill) and a site with considerably higher rainfall (Lake Bennett) to test the hypothesis that the communities at the higher rainfall site would be more diverse. A total of 153 cyanobacteria operational taxonomic units (OTUs) were identified, and only 50 of those were found at both sites. Of these, only two were core OTUs, as defined as being present in ≥90% of samples, highlighting the extreme differences in the cyanobacterial communities at the two sites. At Wave Hill, we compared the composition of the cyanobacterial components under two different rock types (quartz and prehnite) to determine if the different minerals would result in different hypolithic communities, but no differences were found. Of the 42 core OTUs found at Wave Hill, 22 (52%) were shared between the two rock types. As hypothesised, the diversity of both cyanobacteria and eukaryotes in the hypolithic communities was significantly higher at Lake Bennett. Some hypolithic communities were thin and tightly adhered to the rock surface, but others were thicker and could be peeled off the rock in sheets. However, the two types were not significantly different in OTU composition. Metazoans, primarily nematodes, were ubiquitous, raising the possibility that nematodes may act as vectors to transport the components of hypolithic communities from rock to rock as a mechanism of colonization.
- extremophiles,
- hypolithic cyanobacteria,
- nematodes as vectors,
- microbial community,
- semi-arid zone,
- tropical,
- quartz
Citation: Susannah P. Guenther, Karen S. Gibb, Alea M. Rose, Mirjam Kaestli, Keith A. Christian. Differences in structure of northern Australian hypolithic communities according to location, rock type, and gross morphology[J]. AIMS Microbiology, 2018, 4(3): 469-481. doi: 10.3934/microbiol.2018.3.469

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Abstract

Hypolithic communities (under translucent rocks) were compared between a semi-arid site (Wave Hill) and a site with considerably higher rainfall (Lake Bennett) to test the hypothesis that the communities at the higher rainfall site would be more diverse. A total of 153 cyanobacteria operational taxonomic units (OTUs) were identified, and only 50 of those were found at both sites. Of these, only two were core OTUs, as defined as being present in ≥90% of samples, highlighting the extreme differences in the cyanobacterial communities at the two sites. At Wave Hill, we compared the composition of the cyanobacterial components under two different rock types (quartz and prehnite) to determine if the different minerals would result in different hypolithic communities, but no differences were found. Of the 42 core OTUs found at Wave Hill, 22 (52%) were shared between the two rock types. As hypothesised, the diversity of both cyanobacteria and eukaryotes in the hypolithic communities was significantly higher at Lake Bennett. Some hypolithic communities were thin and tightly adhered to the rock surface, but others were thicker and could be peeled off the rock in sheets. However, the two types were not significantly different in OTU composition. Metazoans, primarily nematodes, were ubiquitous, raising the possibility that nematodes may act as vectors to transport the components of hypolithic communities from rock to rock as a mechanism of colonization.

References

[1]	Cowan DA, Khan N, Pointing SB, et al. (2010) Diverse hypolithic refuge communities in the McMurdo Dry Valleys. Antarct Sci 22: 714–720. doi: 10.1017/S0954102010000507
[2]	Ferrenberg S, Tucker CL, Reed SC (2017) Biological soil crusts: diminutive communities of potential global importance. Front Ecol Environ 5: 160–167. doi: 10.3389/fevo.2017.00160
[3]	Tomitani A, Knoll AH, Cavanaugh CM, et al. (2006) The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. P Natl Acad Sci USA 103: 5442–5447. doi: 10.1073/pnas.0600999103
[4]	Makhalanyane TP, Valverde A, Birkeland NK, et al. (2013) Evidence for successional development in Antarctic hypolithic bacterial communities. ISME J 7: 2080–2090. doi: 10.1038/ismej.2013.94
[5]	Khan N, Tuffin M, Stafford W, et al. (2011) Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica. Polar Biol 34: 1657–1668. doi: 10.1007/s00300-011-1061-7
[6]	Tracy CR, Streten-Joyce C, Dalton R, et al. (2010) Microclimate and limits to photosynthesis in a diverse community of hypolithic cyanobacteria in northern Australia. Environ Microbiol 12: 592–607. doi: 10.1111/j.1462-2920.2009.02098.x
[7]	Warren-Rhodes KA, McKay CP, Boyle LN, et al. (2013) Physical ecology of hypolithic communities in the central Namib Desert: the role of fog, rain, rock habitat, and light. J Geophys Res-Biogeo 118: 1451–1460. doi: 10.1002/jgrg.20117
[8]	McKay CP (2016) Water sources for cyanobacteria below desert rocks in the Negev Desert determined by conductivity. Global Ecol Conserv 6: 145–151. doi: 10.1016/j.gecco.2016.02.010
[9]	Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10: 551–562. doi: 10.1038/nrmicro2831
[10]	Cowan DA, Pointing SB, Stevens MI, et al. (2011) Distribution and abiotic influences on hypolithic microbial communities in an Antarctic Dry Valley. Polar Biol 34: 307–311. doi: 10.1007/s00300-010-0872-2
[11]	Stomeo F, Valverde A, Pointing SB, et al. (2013) Hypolithic and soil microbial community assembly along an aridity gradient in the Namib Desert. Extremophiles 17: 329–337. doi: 10.1007/s00792-013-0519-7
[12]	Valverde A, Makhalanyane TP, Seely M, et al. (2015) Cyanobacteria drive community composition and functionality in rock-soil interface communities. Mol Ecol 24: 812–821. doi: 10.1111/mec.13068
[13]	Chan Y, Lacap DC, Lau MC, et al. (2012) Hypolithic microbial communities: between a rock and a hard place. Environ Microbiol 14: 2272–2282. doi: 10.1111/j.1462-2920.2012.02821.x
[14]	Bates ST, Cropsey GW, Caporaso JG, et al. (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microb 77: 1309–1314. doi: 10.1128/AEM.02257-10
[15]	Loudon AH, Woodhams DC, Parfrey LW, et al. (2014) Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). ISME J 8: 830–840. doi: 10.1038/ismej.2013.200
[16]	Apprill A, Robbins J, Eren AM, et al. (2014) Humpback whale populations share a core skin bacterial community: towards a health index for marine mammals? PLoS One 9: e90785. doi: 10.1371/journal.pone.0090785
[17]	Bureau of Meteorology, Australian Government. Available from: http://www.bom.gov.au.
[18]	Qiagen, PowerBiofilm DNA Isolation Kit Sample. MO BIO Laboratories, 2017. Available from: www.mobio.com.
[19]	Park SY, Jang SH, Oh SO, et al. (2014) An easy, rapid, and cost-effective method for DNA extraction from various lichen taxa and specimens suitable for analysis of fungal and algal strains. Mycobiology 42: 311–316. doi: 10.5941/MYCO.2014.42.4.311
[20]	Miller SR, Augustine S, Le Olson T, et al. (2005) Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. P Nat Acad Sci USA 102: 850–855.
[21]	Baker JA, Entsch B, McKay DB (2003) The cyanobiont in an Azolla fern is neither Anabaena nor Nostoc. FEMS Microbiol Lett 229: 43–47. doi: 10.1016/S0378-1097(03)00784-5
[22]	Hadziavdic K, Lekang K, Lanzen A, et al. (2014) Characterization of the 18S rRNA gene for designing universal eukaryote specific primers. PLoS One 9: e87624. doi: 10.1371/journal.pone.0087624
[23]	Caporaso JG, Kuczynski J, Stombaugh J, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336. doi: 10.1038/nmeth.f.303
[24]	Christian K, Kaestli M, Gibb K (2017) Spatial patterns of hypolithic cyanobacterial diversity in Northern Australia. Ecol Evol 2017: 1–11.
[25]	Lacap-Bugler DC, Lee KK, Archer S, et al. (2017) Global diversity of desert hypolithic cyanobacteria. Front Microbiol 8: 867. doi: 10.3389/fmicb.2017.00867
[26]	Smith HD, Baqué M, Duncan AG, et al. (2014) Comparative analysis of cyanobacteria inhabiting rocks with different light transmittance in the Mojave Desert: a Mars terrestrial analogue. Int J Astrobiol 13: 271–277. doi: 10.1017/S1473550414000056
[27]	Komárek J (2007) Phenotype diversity of the cyanobacterial genus Leptolyngbya in the maritime Antarctic. Pol Polar Res 28: 211–231.
[28]	Gokul JK, Valverde A, Tuffin M, et al. (2013) Micro-eukaryotic diversity in hypolithons from Miers Valley, Antarctica. Biology 2: 331–340. doi: 10.3390/biology2010331
[29]	Gadd GM (2017) New horizons in geomycology. Environ Microbiol Rep 9: 4–7. doi: 10.1111/1758-2229.12480
[30]	Boer W, Folman LB, Summerbell RC, et al. (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29: 795–811. doi: 10.1016/j.femsre.2004.11.005
[31]	Belnap J (2001) Microbes and microfauna associated with biological soil crusts, In: Belnap J, Lange OJ, Editors, Biological soil crusts: structure, function, and management, Ecological studies (analysis and synthesis), Berlin: Springer, 167–174.
[32]	Makhalanyane TP, Valverde A, Lacap DC, et al. (2013) Evidence of species recruitment and development of hot desert hypolithic communities. Environ Microbiol Rep 5: 219–224. doi: 10.1111/1758-2229.12003
[33]	Lacap DC, Lau MC, Pointing SB (2011) Biogeography of prokaryotes, In: Fontaneto D, Editor, Biogeography of microscopic organisms: Is everything small everywhere? Cambridge: Cambridge University Press, 35–42.
[34]	Carini P, Marsden PJ, Leff JW, et al. (2016) Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol 2: 16242.
[35]	Demmig-Adams B, Máguas C, Adams WW, et al. (1990) Effect of high light on the efficiency of photochemical energy conversion in a variety of lichen species with green and blue-green phycobionts. Planta 180: 400–409. doi: 10.1007/BF01160396
[36]	Demmig-Adams B, Adams WW, Green TGA, et al. (1990) Differences in the susceptibility to light stress in two lichens forming a phycosymbiodeme, one partner possessing and one lacking the xanthophyll cycle. Oecologia 84: 451–456. doi: 10.1007/BF00328159
[37]	Bahl J, Lau MC, Smith GJ, et al. (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2: 163. doi: 10.1038/ncomms1167
[38]	Pointing SB (2016) Hypolithic communities, In: Weber B, Büdel B, Belnap J, Editors, Biological soil crusts: An organizing principle in drylands, Switzerland: Springer International Publishing, 199–213.
[39]	Warren-Rhodes KA, Rhodes KL, Liu S, et al. (2007) Nanoclimate environment of cyanobacterial communities in China's hot and cold hyperarid deserts. J Geophys Res-Biogeo 112: G01016.
[40]	Ingham RE, Trofymow JA, Ingham ER, et al. (1985) Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol Monogr 55: 119–140. doi: 10.2307/1942528

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