Abstract
Microbes are ubiquitous residents of the atmosphere, including the air that we breathe. They are also widely present in terrestrial, marine, and aquatic environments. Typical microbes include viruses, fungi, archaea, bacteria, algae, and bryophytes. Many are of edaphic origin and play significant ecological roles in the soil. Propagules are exceedingly lightweight and small, generally measured in microns (millionths of a meter). Propagules achieve airborne status in the wind, where they may travel from a few millimeters to thousands of kilometers. Most have been recorded at least as high as the stratosphere. While airborne, microbes may pass through multiple generations. Microbes in the atmosphere are often accompanied by vast clouds of dust. They perform a variety of essential functions such as raindrop and snowflake condensation nuclei, without which there would be little or no precipitation. It is important to realize that all solid things that are carried up into the atmosphere must eventually fall back down to the Earth. When precipitated or deposited back onto the Earth, they may land on and occupy any surface, including trees and other plants where they become epiphytic residents. They have been documented on broad-leaved and needle-leaved trees from deserts to tropical rainforests. If they land on bare soil, they often participate in biological soil crusts that are important for soil stabilization and for water and nutrient cycling.
Introduction
Microbes are nearly ubiquitous in the atmosphere, including in the air that we and other animals breathe. It has been estimated that billions of microbes are descending from the atmosphere at all times of every day (Weisberger, 2018). Typical microbes include viruses, fungi (free-living, lichenized, and mycorrhizal), archaea, bacteria (cyanobacteria, chemoheterotrophic, and diazotrophic), algae including diatoms, and bryophytes (mosses, liverworts, and stoneworts) (Koskella, 2020; Warren and St Clair, 2021). Some microbes reproduce sexually, but most rely primarily on asexual means of reproduction (Warren et al., 2019). Common forms of asexual reproduction among microorganisms include replication, fragmentation, binary fission, cloning, budding, mitotic cell division, asexual sporogenesis, etc. Many of the asexual propagules, and even some of the mature microorganisms are very small, measured in microns (millionths of a meter). Given their small size and weight, microbes and/or their propagules are easily lifted into the atmosphere (Després et al., 2012; Fröhlich-Nowoisky et al., 2016) at least as high as the stratosphere (DasSarma et al., 2020). They are dispersed aerially over extensive distances (Mayol et al., 2017; Reche et al., 2018), including intercontinentally and interhemispherically (Prospero et al., 2005). Microbes are often accompanied by vast clouds of dust from the Earth’s arid areas (Griffin, 2020; Hu et al., 2020).
As microbes and their propagules return to the Earth’s surface, they may be deposited onto bare soil where they can be incorporated into biological soil crusts (Belnap and Lange, 2001). Where bare soil is absent, as in tropical rainforests, the microorganisms occupy the duff or litter layer (Tripathi et al., 2016). Deposited microbes are very abundant, ranging up to 107 living cells of bacteria alone per square centimeter of surface area (Lindow and Brandl, 2003). Airborne microorganisms may alternatively fall onto lava beds (Lavoie et al., 2017), mine tailings (Gypser et al., 2016), or sand dunes (Smith et al., 2004). They may land on bodies of freshwater (Benson et al., 2019) or saltwater (Ul-Hasan et al., 2019). Some may land on snow (Yakimovich et al., 2020), glaciers (Anesio et al., 2017), rocks (Coleine et al., 2021), stone monuments (Li et al., 2016), gravestones (Villanueva et al., 2019), building roofs and facades (Barberán et al., 2015), or animals (Kaup et al., 2021). Others may be inhaled by humans or other animals (Barberán et al., 2015).
Given the theme of this special issue, many microbes and/or their propagules are known to fall from the atmosphere and land on trees where they become epiphytic residents of the phyllosphere, i.e., the aboveground parts of plants exposed to the atmosphere (Koskella, 2020). It can be logically concluded that all plants have epiphytic microbes. Microorganisms have been documented on coniferous trees and shrubs (Neitlich and McCune, 1997; Sevgi et al., 2019) and broad-leaved trees and shrubs (Wallace et al., 2018; Herrmann et al., 2021), fruit trees (Michavila et al., 2017; Janakiev et al., 2019), and nut trees (Pardatscher and Schweigkofler, 2009; Valverde et al., 2017).
In addition to trees, all other plants have a phyllosphere occupied by microorganisms (Partida-Martínez and Heil, 2011), including grasses and grains (Aydogan et al., 2020; Bowsher et al., 2021), ferns (Jackson et al., 2006), vegetables, fruits, and ornamental flowers (Lopez-Velasco et al., 2011; Mamphogoro et al., 2020), as well as cacti and other desert plants (Fonseca-Garcia et al., 2016; Flores-Nuñez et al., 2020). This includes trees and other plants in all climates from tropical rain forests (Kim et al., 2012), to hyperarid deserts (Al-Ashhab et al., 2021), to frigid areas such as Antarctica (Cid et al., 2017). Epiphytic microbes are even known to occur on emergent seagrass (Agawin et al., 2016). While microbes are precipitated onto exposed tree and other plant surfaces, their arrival my vary spatially and seasonally (Lighthart, 1997; Grady et al., 2019).
Functional Roles of Epiphytic Microbes
Epiphytic microorganisms are dispersed passively by wind (Cusimano et al., 2016) and are often accompanied by great clouds of dust (Gannet Hallar et al., 2011). However, as dust particles coalesce and become heavier, and as windspeeds subside, the airborne microorganisms and accompanying dust particles are precipitated back to Earth (Itani and Smith, 2016).
Epiphytic microbes may have either positive or negative impacts on their hosts (Rastogi et al., 2013). Bacteria, fungi, and viruses are often antagonistic pathogens, although some may act as mutualists of the host, promoting plant growth and tolerance of environmental stressors (Stone et al., 2018). As an example, the bacterium Pseudomonas syringae, a well-known plant pathogen, is also a biocontrol against plant viruses and other plant bacteria (Passera et al., 2019). Epiphytic microorganisms also fix or consolidate plant nutrients, particularly nitrogen (Fürnkranz et al., 2008), thus promoting growth of the host plant. Phyllosphere microorganisms can promote plant growth in other ways as well (Wagi and Ahmed, 2017; Yurimoto et al., 2021). Phyllosphere bacteria may also alter susceptibility to insect herbivory (Wielkopolan and Obrȩpalska-Stȩplowska, 2016). Others have been shown to induce tolerance to drought stress (Kumar Devarajan et al., 2021).
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Statements
Author contributions
The author confirms being the sole contributor of this work and has approved it for publication.
Conflict of interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1
Agawin N. S. R. Ferriol P. Cryer C. Alcon E. Busquets A. Sintes E. et al (2016). Significant nitrogen fixation activity associated with the phyllosphere of Mediterranean seagrass Posidonia oceanica: first report.Mar. Ecol. Prog. Ser.55153–62. 10.3354/meps11755
2
Al-Ashhab A. Meshner S. Alexander-Shani R. Dimerets H. Brandwein M. Bar-Lavan Y. et al (2021). Temporal and spatial changes in phyllosphere microbiome of acacia trees growing in arid environments.Front. Microbiol.12:656269. 10.3389/fmicb.2021.656269
3
Anesio A. M. Lutz S. Chrismas N. A. M. Benning L. G. (2017). The microbiome of glaciers and ice sheets.NPJ Biofilms Microbiomes3:10. 10.1038/s41522-017-0019-0
4
Aydogan E. L. Budich O. Hardt M. Choi Y. H. Jansen-Willems A. B. Moser G. et al (2020). Global warming shifts the composition of the abundant bacterial phyllosphere microbiota as indicated by a cultivation-dependent and independent study of the grassland phyllosphere of a long-term warming field experiment.FEMS Microbiol. Ecol.96:fiaa087. 10.1093/femsec/fiaa087
5
Barberán A. Ladau J. Leff J. W. Pollard K. S. Menninger H. L. Dunn R. R. et al (2015). Continental-scale distributions of dust-associated bacteria and fungi.PNAS1125756–5761. 10.1073/pnas.1420815112
6
Belnap J. Lange O. L. (2001). Biological Soil Crusts: Structure, Function, and Management.Berlin: Springer-Verlag, 503.
7
Benson J. Hanion R. Seifried T. M. Baloh P. Powers C. W. Grothe H. et al (2019). Microorganisms collected from the surface of freshwater lakes using a drone water sampling system (DOWSE).Water11:157. 10.3390/w11010157
8
Bowsher A. W. Benucci G. M. N. Bonito G. Shade A. (2021). Seasonal dynamics of core fungi in the switchgrass phyllosphere, and co-occurrence with leaf bacteria.Phytobiomes J.560–68. 10.1094/pbiomes-07-20-0051-r
9
Cid F. P. Inostroza N. G. Graether S. P. Bravo L. A. Jorquera M. A. (2017). Bacterial community structures and ice recrystallization inhibition activity of bacteria isolated from the phyllosphere of the Antarctic vascular plant Deschampsia antarctica.Polar Biol.401319–1331. 10.1007/s00300-016-2036-5
10
Coleine C. Selbmann L. Pombuppa N. Stajich J. E. (2021). Amplicon sequencing of rock-inhabiting microbial communities from Joshua Tree National Park, USA.Microb. Res. Announc.10:e0049421. 10.1128/MRA.00494-21
11
Cusimano C. A. Massa B. Morganti M. (2016). Importance of meteorological variables for aeroplankton dispersal in an urban environment.Ital. J. Zool.83263–269. 10.1080/11250003.2016.1171915
12
DasSarma P. Antunes A. Simönes M. F. DasSarma S. (2020). Earth’s stratosphere and microbial life.Curr. Issues Mol. Biol.38197–244. 10.21775/cimb.038.197
13
Després V. R. Huffman J. A. Burrows S. M. Hoose C. Safatov A. S. Buryak G. et al (2012). Primary biological aerosol particles in the atmosphere: a review.Tellus B Chem. Phys. Meteorol.64:1. 10.3390/atmos9010001
14
Flores-Nuñez V. M. Fonseca-Garcia C. Desgarennes D. Eloe-Fadrosh E. Woyke T. Partida-Martínez L. P. (2020). Functional signatures of the epiphytic prokaryotic microbiome of agaves and cacti.Front. Microbiol.10:3044. 10.3389/fmicb.2019.03044
15
Fonseca-Garcia C. Coleman-Derr D. Garrido E. Visel A. Tringe S. G. Partida-Martínez L. P. (2016). The cacti microbiome: interplay between habitat-filtering and host-specificity.Front. Microbiol.7:150. 10.3389/fmicb.2016.00150
16
Fröhlich-Nowoisky J. Kampf C. J. Weber B. Huffman J. A. Pöhlker C. Andreaea M. O. et al (2016). Bioaerosols in the earth system: climate, health, and ecosystem interactions.Atmos. Res.182346–376. 10.1016/j.atmosres.2016.07.018
17
Fürnkranz M. Wanek W. Richter A. Abell G. Rasche F. Sessitsch A. (2008). Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of costa rica.ISME J.2561–570. 10.1038/ismej.2008.14
18
Gannet Hallar A. Chirokova G. McCubbin I. Painter T. H. Wiedinmyer C. Dodson C. (2011). Atmospheric bioaerosols transported via dust storms in the western United States.Geophys. Res. Lett.38:L17801.
19
Grady K. L. Sorensen J. W. Stopnisek N. Guittar J. Shade A. (2019). Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops.Nat. Commun.10:4135. 10.1038/s41467-019-11974-4
20
Griffin D. W. (2020). Atmospheric movement of microorganisms in clouds of desert dust and implications for human health.Clin. Microbiol. Rev.20459–477. 10.1128/CMR.00039-06
21
Gypser S. Veste M. Fischer T. Lange P. (2016). Infiltration and water retention of biological soil crusts on reclaimed soils of former open-cast lignite mining sites in Brandenburg, north-east Germany.J. Hydrol. Hydromech.641–11.
22
Herrmann M. Geesink P. Richter R. Küsel K. (2021). Canopy position has a stronger effect than tree species identity on phyllosphere bacterial diversity in a floodplain hardwood forest.Microb. Ecol.81157–168. 10.1007/s00248-020-01565-y
23
Hu W. Murata K. Fan C. Huang S. Matsusaki H. Fu P. et al (2020). Abundance and viability of particle-attached and free-floating bacteria in dusty and nondusty air.Biogeosciences174477–4487. 10.5194/bg-17-4477-2020
24
Itani G. N. Smith C. A. (2016). Dust rains deliver diverse assemblages of microorganisms to the eastern Mediterranean.Sci. Rep.16:22657. 10.1038/srep22657
25
Jackson E. F. Echlin H. L. Jackson C. R. (2006). Changes in the phyllosphere community of the resurrection fern, Polypodium polypodioides, associated with rainfall and wetting.FEMS Microb. Ecol.58236–246. 10.1111/j.1574-6941.2006.00152.x
26
Janakiev T. Dimkić I. Unković N. Ljaljević Grbić M. Opsenica D. Gašić U. et al (2019). Phyllosphere fungal communities of plum and antifungal activity of indigenous phenazine-producing Pseudomonas synxantha against Monilinia laxa.Front. Microbiol.10:2287. 10.3389/fmicb.2019.02287
27
Kaup M. Trull S. Hom E. F. Y. (2021). On the move: sloths and their epibionts as model mobile ecosystems.Biol. Rev.962638–2660. 10.1111/brv.12773
28
Kim M. Singh D. Lai-Hoe A. Go R. Rahim R. A. Ainuddin A. N. et al (2012). Distinctive phyllosphere bacterial communities in tropical trees.Microb. Ecol.63674–681. 10.1007/s00248-011-9953-1
29
Koskella B. (2020). The phyllosphere.Curr. Biol.30R1096–R1114.
30
Kumar Devarajan A. Muthukrishanan G. Truu J. Truu M. Ostonen I. Kizhaeral S. et al (2021). The foliar application of rice phyllosphere bacteria induces drought-stress tolerance in Oryza sativa (L.).Plants10:387. 10.3390/plants10020387
31
Lavoie K. H. Winter A. S. Read K. J. H. Hughes E. M. Spilde M. N. Northrup D. E. (2017). Comparison of bacterial communities from lava cave microbial mats to overlying surface lava cave microbial mats to overlying surface soils from Lava Beds National Monument, USA.PLoS One12:e0169339. 10.1371/journal.pone.0169339
32
Li Q. Zhang B. He Z. Yang X. (2016). Distribution and diversity of bacteria and fungi colonization in stone monuments analyzed by high-throughput sequencing.PLoS One11:e0163287. 10.1371/journal.pone.0163287
33
Lighthart B. (1997). The ecology of bacteria in the alfresco atmosphere.FEMS Microbiol. Ecol.23263–274. 10.1016/s0168-6496(97)00036-6
34
Lindow S. E. Brandl M. T. (2003). Microbiology of the phyllosphere.Appl. Environ. Microbiol.691875–1883.
35
Lopez-Velasco G. Welbaum G. E. Falkinham J. O. III Ponder M. A. (2011). Phyllosphere bacterial community structure of spinach (Spinacia oleracea) as affected by cultivar and environmental conditions at time of harvests. Diversity13, 721–738.
36
Mamphogoro T. P. Maboko M. M. Babalola O. O. Aiyegoro O. A. (2020). Bacterial communities associated with the surface of fresh sweet pepper (Capsicum annuum) and their potential as biocontrol.Sci. Rep.10:8560.
37
Mayol E. Arrieta J. M. Jímenez M. A. Martínez-Asensio A. Garcias-Bonet N. Dachs J. et al (2017). Long-range transport of airborne microbes over the global tropical and subtropical ocean.Nat. Commun.8:21. 10.1038/s41467-017-00110-9
38
Michavila G. Adler C. De Gregorio P. R. Lami M. J. Caram Di Santo M. C. Zenoff A. M. et al (2017). Pseudomonas protegens CS1 from the lemon phyllosphere as a candidate for citrus canker biocontrol agent.Plant Biol. (Stuttgart)19608–617. 10.1111/plb.12556
39
Neitlich P. N. McCune B. (1997). Hotspots of epiphytic lichen diversity in two young managed forests.Conserv. Biol.11172–182. 10.1046/j.1523-1739.1997.95492.x
40
Pardatscher R. Schweigkofler W. (2009). Microbial biodiversity associated with the walnut Juglans regia L. in South Tyrol (Italy).Mitt. Klosterneuburg5924–30.
41
Partida-Martínez l. P Heil M. (2011). The microbe-free plant: fact or artifact?Front. Plant Sci.2:100. 10.3389/fpls.2011.00100
42
Passera A. Compant S. Casati P. Maturo M. G. Battell G. Quaglino F. et al (2019). Not just a pathogen? Description of a plant-beneficial Pseudomonas syringae strain.Front. Microbiol.10:1409. 10.3389/fmicb.2019.01409
43
Prospero J. M. Blades E. Mathison G. Naidu R. (2005). Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust.Aerobiologia211–19. 10.1007/s10453-004-5872-7
44
Rastogi G. Coaker G. L. Leveau J. H. J. (2013). New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches.FEMS Microbiol. Lett.3481–10. 10.1111/1574-6968.12225
45
Reche I. D’Orta G. Mladenov N. Winget D. M. Suttle C. A. (2018). Deposition rates of viruses and bacteria above the atmospheric boundary layer.ISME J.121154–1162. 10.1038/s41396-017-0042-4
46
Sevgi E. Yalçın Yılmaz O. Çobanoğlu Özyiğitoǧlu G. Barış Tecimen H. Sevgi O. (2019). Factors influencing epiphytic lichen species distribution in a managed Mediterranean Pinus nigra Arnold Forest.Diversity11:59. 10.3390/d11040059
47
Smith S. M. Abed R. M. M. Garcia-Pichel F. (2004). Biological soil crusts of sand dunes in Cape Cod National Seashore, Massachusetts, USA.Microb. Ecol.38200–208. 10.1007/s00248-004-0254-9
48
Stone B. W. G. Weingarten E. A. Jackson C. R. (2018). The role of the phyllosphere microbiome in plant health and function.Annu. Plant Rev. Online11–24.
49
Tripathi B. M. Song W. Slik J. W. F. Sukri R. S. Jaafar S. Dong K. et al (2016). Distinctive tropical forest variants have unique soil microbial communities, but not always low microbial diversity.Front. Microbiol.7:376. 10.3389/fmicb.2016.00376
50
Ul-Hasan S. Bowers R. M. Figueroa-Montiel A. Licea-Navarro A. F. Beman J. M. Woyke T. et al (2019). Community ecology across bacteria, archaea and microbial eukaryotes in the sediment and seawater of coastal Puerto Nuevo, Baja California.PLoS One14:eO212355. 10.1371/journal.pone.0212355
51
Valverde A. González-Tirante M. Medina-Sierra M. Rivas R. Santa-Regina I. Igual J. M. (2017). Culturable bacterial diversity from the chestnut (Castanea sativa Mill.) phyllosphere and antagonism against the fungi causing the chestnut blight and ink diseases.AIMS Microbiol.3293–314. 10.3934/microbiol.2017.2.293
52
Villanueva C. Garvey A. D. Hašler P. Dvořák P. Pouličková A. Norwich A. R. et al (2019). Descriptions of Brasilonema geniculatum and Calothrix dumus (Nostocales, Cyanobacteria): two new taxa isolated from cemetery tombstones.Phytotaxa3871–20. 10.11646/phytotaxa.387.1.1
53
Wagi S. Ahmed A. (2017). Phyllosphere plant growth promoting bacteria.J. Bacteriol. Mycol.5215–216.
54
Wallace J. LaForest-LaPointe I. Kembel S. W. (2018). Variation in the leaf and root microbiome of sugar maple (Acer saccharum) at an elevational range limit.PeerJ6:e5293. 10.7717/peerj.5293
55
Warren S. D. St Clair L. L. (2021). Atmospheric transport and mixing of biological soil crust microorganisms.AIMS Environ. Sci.8498–516ȩ.
56
Warren S. D. St. Clair L. L. Stark L. R. Lewis L. A. Pombubpa N. Kurbessoian T. et al (2019). Reproduction and dispersal of biological soil crust organisms.Front. Ecol. Evol.7:344. 10.3389/fevo.2019.00344
57
Weisberger M. (2018). Billions of viruses are falling to earth right now (but that isn’t why you have the flu).Live Sci.07:2018.
58
Wielkopolan B. Obrȩpalska-Stȩplowska A. (2016). Three-way interaction among plants, bacteria, and coleopteran insects.Plants244313–332.
59
Yakimovich K. M. Engstrom C. B. Quarmby L. M. (2020). Alpine snow algae microbiome diversity in the coast British Columbia.Front. Microbiol.11:1721. 10.3389/fmicb.2020.01721
60
Yurimoto H. Shiraishi K. Sakai Y. (2021). Physiology of methylotrophs living in the phyllosphere.Microorganisms9:809. 10.3390/microorganisms9040809
Summary
Keywords
viruses, fungi, archaea, bacteria, algae, bryophytes, aerobiology
Citation
Warren SD (2022) Microorganisms of the Phyllosphere: Origin, Transport, and Ecological Functions. Front. For. Glob. Change 5:843168. doi: 10.3389/ffgc.2022.843168
Received
25 December 2021
Accepted
06 April 2022
Published
11 May 2022
Volume
5 - 2022
Edited by
Paolo Giordani, University of Genoa, Italy
Reviewed by
Rebecca McDougal, New Zealand Forest Research Institute Limited (Scion), New Zealand
Updates
Copyright
© 2022 Warren.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Steven D. Warren, steven.warren@usda.gov
This article was submitted to Temperate and Boreal Forests, a section of the journal Frontiers in Forests and Global Change
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.